Recent advances in understanding of the epigenetic regulation of plant regeneration

Xuemei Liu; Kehui Zhu; Jun Xiao

doi:10.1007/s42994-022-00093-2

Recent advances in understanding of the epigenetic regulation of plant regeneration

Liu, Xuemei; Zhu, Kehui; Xiao, Jun 2023-03-01 00:00:00 aBIOTECH https://doi.org/10.1007/s42994-022-00093-2 aBIOTECH REVIEW Recent advances in understanding of the epigenetic regulation of plant regeneration 1,2& 1,2 1,2,3& Xuemei Liu , Kehui Zhu , Jun Xiao Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China CAS-JIC Centre of Excellence for Plant and Microbial Science (CEPAMS), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China Received: 27 October 2022 / Accepted: 27 December 2022 Abstract Ever since the concept of ‘‘plant cell totipotency’’ was ﬁrst proposed in the early twentieth century, plant regeneration has been a major focus of study. Regeneration-mediated organogenesis and genetic transformation are important topics in both basic research and modern agriculture. Recent studies in the model plant Arabidopsis thaliana and other species have expanded our understanding of the molecular regulation of plant regeneration. The hierarchy of transcriptional regulation driven by phytohormone signaling during regeneration is associated with changes in chromatin dynamics and DNA methylation. Here, we summarize how various aspects of epigenetic regulation, including histone modiﬁcations and variants, chromatin accessibility dynamics, DNA methylation, and microRNAs, modulate plant regeneration. As the mechanisms of epigenetic regulation are conserved in many plants, research in this ﬁeld has potential applications in boosting crop breeding, especially if coupled with emerging single-cell omics technologies. Keywords Plant regeneration, Epigenetic regulation, Arabidopsis, Crop breeding INTRODUCTION callus differentiation in tobacco (Nicotiana tabacum) (Skoog and Miller 1957), providing experimental tools From unicellular green algae to angiosperms, plants are and a conceptual framework for exploring the functions highly regenerative, meaning that new organs or whole of phytohormones and their interactions during regen- bodies can be rebuilt following injury (Ikeuchi et al. eration (Birnbaum and Alvarado 2008). Plant tissue 2016, 2019). Research on regeneration can be traced culture has been widely used in both basic research and back to Gottlieb Haberlandt’s description of totipotency agriculture and provides an excellent system for proposed in the early twentieth century (Haberlandt studying plant organogenesis and somatic embryogen- 2003; Krikorian and Berquam 2003; Thorpe 2007). In esis. Strategies that combine tissue culture and genome 1957, Skoog and Miller demonstrated that the ratio of editing technologies provide opportunities to geneti- exogenous auxin to cytokinin (CK) affects the fate of cally improve crops (Loyola-Vargas and Ochoa-Alejo 2018). Plant regeneration can be divided into two cate- Xuemei Liu and Kehui Zhu have contributed equally. gories: injury-induced regeneration and tissue culture- induced regeneration (Mathew and Prasad 2021). In the & Correspondence: xmliu@genetics.ac.cn (X. Liu), jxiao@genet- former, different regeneration processes occur ics.ac.cn (J. Xiao) The Author(s) 2023 aBIOTECH depending on the type of injury (Ikeuchi et al. 2016). and the expression of WOX5 and WOX7 is restricted to When the meristem is partially damaged, the plant will the stem cell niche (Hu and Xu 2016;Xu 2018; Jing et al. reconstruct the meristem, whereas when the meristem 2020). In addition, PLETHORA 1 (PLT1), PLT2, SCARE- is completely absent, the plant will grow axillary shoots CROW (SCR), and SHORT ROOT (SHR) are essential for or lateral roots. Some plant species, such as those in the quiescent center speciﬁcation and stem cell activity in Crassulaceae and Gesneriaceae families, can undergo de the RAM (Della Rovere et al. 2015; Shimotohno et al. novo organogenesis to form new shoots or roots from 2018). However, under the induction of CK in SIM, the cut sites (Ikeuchi et al. 2016). Other plants, however, callus differentiates into shoots. First, the expression of require tissue culture to regenerate the entire plant. CUP-SHAPED COTYLEDON1 (CUC1) and CUC2 in callus is Injury activates a range of genes, including cell cycle spatially reorganized to mark promeristem regions, and genes, genes involved in CK synthesis and responses, PIN-FORMED 1 (PIN1) is induced by CUCs to determine and genes encoding transcription factors (TFs) of the the future locations of shoot progenitors (Hibara et al. AP2/ERF family (Ikeuchi et al. 2017). WOUND INDUCED 2003; Daimon et al. 2003; Gordon et al. 2007; Shin et al. DEDIFFERENTIATION 1 (WIND1) is rapidly induced at 2020). Along with the up-regulation of PIN1, SHOOT the wounding site and promotes cell dedifferentiation to MERISTEMLESS (STM) is expressed in the promeristem form callus via type-B ARR (Iwase et al. 2011). Another to maintain shoot meristem activity (Gordon et al. 2007; gene in the AP2/ERF family, ETHYLENE RESPONSE Shin et al. 2020). In addition, type-B ARRs in the CK FACTOR 115 (ERF115), promotes reconstitution of the signaling pathway, including ARABIDOPSIS RESPONSE stem cell niche after root tip excision (Heyman et al. REGULATOR 1 (ARR1), ARR2, ARR10, and ARR12, 2016). directly bind to and activate WUSCHEL (WUS), which Tissue culture-induced regeneration can be divided directs the shoot apical meristem (SAM) formation into three types based on the culture system and program (Negin et al. 2017; Zhang et al. 2017b; Shin regeneration process used: de novo root regeneration, et al. 2020). de novo shoot regeneration, and somatic embryogenesis Unlike de novo root or shoot regeneration, somatic (Mathew and Prasad 2021). Both de novo root regen- embryogenesis leads to the formation of a bipolar eration and shoot regeneration are two-step processes. structure with an apical and basal pole. In Arabidopsis, The explant forms callus on an auxin-rich callus induc- somatic embryogenesis is often induced from 2,4- tion medium (CIM). The callus then differentiates into dichlorophenoxyacetic acid (2,4-D)-treated immature roots on root induction medium (RIM), which contains zygotic embryos at the bent cotyledon stage of devel- little or no auxin, or shoots on CK-rich shoot induction opment (Horstman et al. 2017). Ectopic expression of medium (SIM) (Lardon and Geelen 2020). Regardless of the embryo identity genes LEAFY COTYLEDON 1 (LEC1) the origin of the explant, the process of callus formation (Lotan et al. 1998) and LEC2 (Stone et al. 2001), the induced on CIM follows the root developmental path- meristem identity genes BABY BOOM (BBM) (Boutilier way (Sugimoto et al. 2010), and the identity of the callus et al. 2002) and WUS (Gaj 2004; Chatﬁeld et al. 2013), is similar to that of root primordia (Zhai and Xu 2021). and wound-induced WIND1 (Ikeuchi et al. 2013) indu- During this process, auxin signaling in Arabidopsis ces somatic embryogenesis. (Arabidopsis thaliana) ﬁrst activates WUSCHEL RELA- Plant cells undergo multiple rapid cell fate transitions TED HOMEOBOX 11 (WOX11) and WOX12, which during regeneration, which is accompanied by the transforms the regenerative pericycle or pericycle-like reprogramming of the transcriptome and chromatin cells of the explant into root founder cells (Atta et al. landscape. Cell identity genes, especially TF genes, are 2009; Liu et al. 2014; Sang et al. 2018;Xu 2018). Sub- induced by phytohormones to participate in plant sequently, in the continuous presence of auxin, WOX11/ regeneration (Sang et al. 2018; Ikeuchi et al. 2019; WOX12 activates the expression of WOX5, WOX7, LAT- Sugimoto et al. 2019; Mathew and Prasad 2021). The ERAL ORGAN BOUNDARIES-DOMAIN 16 (LBD16), and expression of these key TF genes is partially regulated LBD29, which in turn transform root founder cells into by various epigenetic regulators. In 2007, Crane and root primordium cells (Hu and Xu 2016;Xu 2018; Liu Gelvin reported that RNAi lines in which 24 genes et al. 2018b). Thus, callus is formed on CIM. encoding epigenetic regulators, including chromatin Subsequently, the ratio of auxin to CK determines the remodeling complexes, DNA methyltransferases, and direction of callus re-differentiation. On RIM, callus various histone modiﬁcation-related enzymes, had been resembling root primordia continues to undergo cell silenced showed altered genetic transformation efﬁ- division and differentiates into a well-organized root ciencies (Crane and Gelvin 2007). Further studies have apical meristem (RAM). During this process, LBD16 uncovered epigenetic dynamics during plant regenera- expression in the root meristem gradually decreases tion and highlighted the importance of the epigenetic The Author(s) 2023 aBIOTECH regulation of key TFs that drive the cell fate transition tissue culture-induced regeneration, and propose future during regeneration (Wang et al. 2020; Xu et al. 2021; directions for better understanding the different layers Wu et al. 2022). Here, we summarize recent advances in of epigenetic regulation of plant regeneration and their understanding the epigenetic regulation of the plant applications in crop breeding. regeneration process (Fig. 1, Table 1), with a focus on Fig. 1 Roles of epigenetic regulators in plant regeneration. Mechanisms of histone methylation (A), histone acetylation (B), DNA methylation (C), and miRNA (D) in regulating plant regeneration. The font color indicates the transcriptional status of the gene, with red representing transcriptional activation and blue representing transcriptional repression. The scissors represent the injury-induced regeneration. The arrows represent activation and the T-ended arrows represent inhibition The Author(s) 2023 aBIOTECH Table 1 Epigenetic regulators of plant regeneration Protein Protein ID Annotation Targets Roles in regeneration References name CLF AT2G23380 H3K27me3 SAW1, SAW2, ATH1, Inhibits somatic embryogenesis; He et al. (2012) methyltransferase TCP10 Promotes callus formation from leaves SWN AT4G02020 H3K27me3 SAW1, SAW2, ATH1, Inhibits somatic embryogenesis; He et al. (2012) methyltransferase TCP10 Promotes callus formation from leaves ATX4 AT4G27910 H3K4me3 ATH1, KANT4, Inhibits callus formation from Lee et al. (2019) methyltransferase SAW1, SAW2, leaves; Promotes shoot TCP10, YAB5 regeneration from callus LDL3 AT4G16310 H3K4me2 CIPK23, GLT1, Promotes shoot regeneration from Ishihara et al. (2019) demethylase UPL4, ARR12 callus ATXR2 AT3G21820 H3K36me3 LBD16, LBD29, Promotes callus formation from Lee et al. methyltransferase ARR5, ARR7 leaves; Inhibits shoot (2017, 2018b, 2021) regeneration from callus ASHR3 AT4G30860 H3K36me3 ARR1, PLT3, WIND3 Promotes wound-induced callus Lee et al. (2020) methyltransferase formation JMJ30 AT3G20810 H3K9me3 LBD16, LBD29 Promote callus formation from Lee et al. (2018a) demethylase leaves AtPRMT5 AT4G31120 H4R3sme2 KRP1 Promotes shoot regeneration from Liu et al. (2016a) methyltransferase callus HAG1 AT3G54610 histone WOX5, SCR, PLT1, Promotes wound-induced callus Kim et al. (2018), acetyltransferase PLT2 formation; Promotes shoot Rymen et al. (2019) regeneration from callus HAG3 AT5G50320 histone NA Promotes wound-induced callus Rymen et al. (2019) acetyltransferase formation HDA19 AT4G38130 histone LEC2 Inhibits somatic embryogenesis Moron´ czyk et al. deacetylases (2022) HDA9 AT3G44680 histone LBD17, LEC1 Inhibits callus formation from (Lee et al. 2016) deacetylases leaves HDT1 AT3G44750 histone BBM, WUS Inhibits callus formation from Lee et al. (2016) deacetylases leaves OsHDA710 Os02g0215200 histone OsARF18, OsARF22 Promote callus formation from Zhang et al. (2020) deacetylases embryos HTR15 AT5G12910 coding H3.15 WOX11 Promotes wound-induced callus Yan et al. (2020) formation; Promotes callus formation from hypocotyls INO80 AT3G57300 chromatin PIN1 Collaborates with histone Kang et al. (2019) remodeling chaperones NRP1/2 to regulate complexes IM and RAM activities PKL AT2G25170 chromatin LEC1, FUS3, ABI3, Facilitates root meristem activity; Aichinger et al. remodeling EMF2, CLF, SWN, Limits embryogenesis (2009, 2011) complexes AP3, AG, FLC BRM AT2G46020 chromatin Cyc81;1, CycB1;3, Maintains the root stem cell niche Yang et al. (2015) remodeling PIN1–4, PIN7 complexes CHR3 AT2G28290 chromatin WUS Maintains the ﬂoral meristem Sun et al. (2019) remodeling complexes MET1 AT5G49160 DNA WUS, ARR1, ARR10, Inhibits shoot regeneration from Liu et al. (2018a), Shim methyltransferase CRY1 callus et al. (2021) DRM1 AT5G15380 DNA WUS Inhibits shoot regeneration from Shemer et al. (2015) methyltransferase callus DRM2 AT5G14620 DNA WUS Inhibits shoot regeneration from Shemer et al. (2015) methyltransferase callus The Author(s) 2023 aBIOTECH Table 1 continued Protein Protein ID Annotation Targets Roles in regeneration References name CMT3 AT1G69770 DNA WUS Inhibits shoot regeneration from Shemer et al. (2015) methyltransferase callus miR156 microRNA SPL9 Promotes shoot regeneration; Zhang et al. (2015), Promotes somatic Long et al. (2018) embryogenesis miR319 microRNA TCP3, TCP4 Inhibits shoot regeneration Yang et al. (2020) miR160 microRNA ARF10 Inhibits callus formation; Inhibits Qiao et al. (2012), Liu shoot regeneration et al. (2016b) miR167 microRNA ARF6, ARF8 Inhibits somatic embryogenesis Arora et al. (2020) miR393 microRNA TIR1, AFB3 Inhibits shoot regeneration; Wo´jcik and Gaj (2016), Inhibits somatic embryogenesis Wang et al. (2018) LAYERS OF EPIGENETIC REGULATION histone has various effects on the transcriptional regu- OF TRANSCRIPTION lation of genes. In general, trimethylation at lysine 27 of histone H3 (H3K27me3) and trimethylation at lysine 9 Gene transcription is regulated at multiple levels. In of histone H3 (H3K9me3) negatively regulate tran- general, trans-acting TFs bind to cis-elements in their scription, whereas trimethylation at lysine 4 of histone target promoters to promote or inhibit gene transcrip- H3 (H3K4me3) and trimethylation at lysine 36 of his- tion. However, in the cellular environment, DNA is tone H3 (H3K36me3) are associated with transcrip- wrapped around histones and packaged into nucleo- tional activation (Xiao et al. 2016). Histone methylation somes, which limits the access of TFs. Transcription dynamics are regulated by ‘‘writers’’ that add methyl factors compete with histones and other chromatin- groups, such as histone lysine methyltransferase binding proteins to bind to DNA (Klemm et al. 2019). (HKMTs) and protein arginine methyltransferases Chromatin remodeling complexes can directly alter (PRMTs), and ‘‘erasers’’ that remove methyl group, such nucleosome composition and interactions, thereby as histone demethylases (HDMs) (Liu et al. 2010). affecting chromatin accessibility (Ojolo et al. 2018). Methylation or acetylation of histone H3 and H4 can H3K27me3 dynamics regulate plant regeneration affect the interactions between histones and DNA, resulting in loose or dense chromatin (Pﬂuger and In Arabidopsis, H3K27me3 is catalyzed by Polycomb Wagner 2007). DNA methylation is also involved in repressive complex 2 (PRC2), which consists of four transcriptional regulation. DNA methylation in promot- subunits. The catalytic subunit Enhancer of zeste ers inhibits gene transcription, whereas DNA methyla- homolog2 (EZH2) is encoded by three functionally tion in gene bodies is mostly associated with independent genes: CURLY LEAF (CLF), SWINGER constitutive expression (Zhang et al. 2018a). Post-tran- (SWN), and MEDEA (MEA). The spatial–temporal-speci- scriptional regulation, such as processes mediated by ﬁc expression of these genes leads to the functional microRNA (miRNA), can also affect gene expression diversiﬁcation of PRC2 (Bieluszewski et al. 2021). (Gibney and Nolan 2010). Instead of exhibiting normal plant architecture, the clf swn double mutant spontaneously forms a callus-like tissue that accumulates neutral lipids and occasionally REGULATION OF PLANT REGENERATION somatic embryo-like structures (Chanvivattana et al. VIA HISTONE MODIFICATIONS AND HISTONE 2004; Ikeuchi et al. 2015). Although auxin failed to VARIANTS induce somatic embryogenesis from wild-type shoots, this treatment induced somatic embryo formation from Histone methylation-regulated plant clf swn shoots (Mozgova´ et al. 2017). This observation regeneration suggests that the loss of function of PRC2 promotes somatic embryogenesis from vegetative tissues in Ara- The lysine or arginine residues of histone tails can be bidopsis. In rice (Oryza sativa), the H3K27me3 levels of modiﬁed by mono-, di- and tri-methylation, which OsWOX6, OsWOX9, OsWOX11, OsPLT3, OsPLT6, and affects transcription by altering the local chromatin OsPLT8 are signiﬁcantly lower in callus than in seedlings state. Methylation of residues at different positions of (Zhao et al. 2020). In peach (Prunus persica), during the The Author(s) 2023 aBIOTECH leaf-to-callus transition, the up-regulation of auxin-re- YAB5 to regain shoot identity (Fig. 1A) (Lee et al. 2019). lated genes PpPIN6 and AUXIN-INDUCED PROTEIN 13 Thus, ATX4-mediated H3K4me3 has dual functions in (PpIAA13) and the lateral root development-related callus induction and the re-differentiation of callus in genes PpLBD1, LATERAL ORGAN BOUNDARIES (PpLOB), Arabidopsis. By contrast, in crops such as wheat (Liu SHI RELATED SEQUENCE 1 (PpSRS1), and LATERAL et al. 2022b) and rice (Zhao et al. 2020), H3K4me3 ROOT PRIMORDIUM 1 (PpLRP1) is accompanied by a deposition increases during immature embryo- or seed- decrease in H3K27me3 levels (Zheng et al. 2022). Fur- induced callus formation, pointing to an opposite role thermore, treatment with the H3K27me3 demethylase for H3K4me3 in promoting callus formation in these inhibitor GSK-J4 signiﬁcantly reduced the rate of callus crops compared to Arabidopsis. This discrepancy might induction in peach (Zheng et al. 2022). In hexaploid be due to the different types of explants used for each wheat (Triticum aestivum), H3K27me3 deceases at species. auxin signaling genes and root meristem formation-re- In general, dimethylation at lysine 4 of histone H3 lated genes such as TaPIN1 and TaLBD17 during the late (H3K4me2) positively regulates gene expression in stage of callus formation from immature embryos (Liu animals (Barski et al. 2007) but is associated with gene et al. 2022b). Thus, the attenuation of H3K27me3 of repression in plants (Liu et al. 2019). LYSINE-SPECIFIC auxin signaling and meristematic-related genes could DEMETHYLASE 1-LIKE 3 (LDL3) accumulates and facilitate their activation and promote callus formation. speciﬁcally erases H3K4me2 marks on genes required By contrast, leaf tissue of the Arabidopsis clf swn mutant for the acquisition of shoot traits during callus forma- failed to form callus on CIM, because leaf identity genes, tion from root cells (Ishihara et al. 2019). Interestingly, such as SAWTOOTH 1 (SAW1), SAW2, ARABIDOPSIS LDL3-mediated removal of H3K4me2 does not imme- THALIANA HOMEOBOX GENE 1 (ATH1), and TCP diately activate target genes, but rather primes genes for DOMAIN PROTEIN 10 (TCP10), cannot be repressed subsequent activation during shoot induction on SIM without PRC2-mediated H3K27me3 deposition during (Ishihara et al. 2019). Accordingly, the competency of dedifferentiation and callus induction (Fig. 1A) (He et al. shoot regeneration is severely impaired in the ldl3 2012). In summary, PRC2-mediated H3K27me3 marks mutant due to its failure to eliminate H3K4me2 on meristematic genes in differentiated tissues to prevent shoot regeneration genes, such as CBL-INTERACTING callus formation, while it is also required to turn off PROTEIN KINASE 23 (CIPK23) and UBIQUITIN-PROTEIN tissue identity genes for the acquisition of pluripotency LIGASE 4 (UPL4) (Ishihara et al. 2019). and to facilitate callus formation. The status of H3K36me3 and H3K9me3 inﬂuences plant Altering H3K4me3 and H3K4me2 affects plant regeneration regeneration Signaling factors in the auxin and CK pathways interact During the leaf-to-callus transition in Arabidopsis, the with histone modiﬁers to regulate gene expression down-regulation of leaf identity genes is also regulated during plant regeneration. The H3K36me3 methyl- by the decrease in H3K4me3 levels. ARABIDOPSIS transferase gene ARABIDOPSIS TRITHORAX-RELATED 2 TRITHORAX 4 (ATX4) (Foroozani et al. 2021) catalyzes (ATXR2) (Lee et al. 2017) and the H3K9me3 demethy- the trimethylation of H3K4 and participates in de novo lase gene JUMONJI C DOMAIN-CONTAINING PROTEIN 30 shoot regeneration from leaf explants (Lee et al. 2019). (JMJ30) (Lee et al. 2018a) are constitutively up-regu- ATX4 is highly expressed in leaves and deposits lated upon callus induction on CIM. The auxin signaling H3K4me3 on the leaf identity genes ATH1, KNOTTED1- factors AUXIN RESPONSE FACTOR 7 (ARF7) and ARF19 LIKE HOMEOBOX GENE 4 (KNAT4), SAW1, SAW2, TCP10, interact with and recruit ATXR2 and JMJ30 to the pro- and YABBY 5 (YAB5) to maintain leaf cell identify. Upon moters of LBD16 and LBD29 and activate their expres- induction on CIM, the expression level of ATX4 decrea- sion to promote the dedifferentiation of leaf explants ses rapidly and remains low throughout callus induc- and callus formation (Fig. 1A) (Lee et al. 2017, 2018a). tion. As a result, the H3K4me3 and expression levels of Notably, both JMJ30-mediated decreases in H3K9me3 leaf identity genes decrease, which results in the loss of and ATXR2-mediated increases in H3K36me3 are leaf cell identity (Lee et al. 2019). Compared to the wild required for the activation of LBDs during the leaf-to- type, atx4 more readily generates callus from leaf tissue callus transition. ATXR2 also promotes root organo- (Lee et al. 2019). ATX4 also affects re-differentiation genesis on a phytohormone-free medium (Lee et al. from callus to shoot tissue. When callus is transferred to 2018b) and inhibits shoot regeneration on SIM (Lee SIM, ATX4 is temporarily up-regulated, and ATX4 re- et al. 2021). The atxr2 mutant shows enhanced shoot deposits H3K4me3 on ATH1, SAW1, SAW2, TCP10, and regeneration from the callus regardless of the origin of The Author(s) 2023 aBIOTECH the explant (Lee et al. 2021). ATXR2 interacts with type- H3 (H3K27ac) accumulate on genes that are up-regu- B ARR1 in the CK signaling pathway to deposit lated by wounding, such as WIND1, ERF113/RAP2.6L, H3K36me3 and activate ARR5 and ARR7 on SIM. ARR5 and LBD (Rymen et al. 2019). The histone acetyltrans- and ARR7 are type-A ARRs that inhibit WUS expression ferases HISTONE ACETYLTRANSFERASE OF THE GNAT and shoot formation (Lee et al. 2021). Therefore, auxin- FAMILY 1 (HAG1) and HAG3 promote callus formation inducible ATXR2 regulates CK signaling and precisely during wounding, as the callus formation rate is signif- controls WUS expression to prevent premature shoot icantly reduced in hag1 and hag3 mutants (Rymen et al. induction. Another H3K36me3 methyltransferase, 2019). HAG1 also promotes the transition of callus to ASH1-RELATED 3 (ASHR3), promotes wound-induced shoots. During de novo shoot regeneration, HAG1 cat- callus formation. Following wounding, ASHR3 is rapidly alyzes the acetylation of WOX5, SCR, PLT1, and PLT2 and activated and deposits H3K36me3 on ARR1, PLT3, and promotes their expression, allowing the callus to WIND3 to promote callus formation (Fig. 1A) (Lee et al. acquire competence for shoot regeneration (Fig. 1B) 2020). (Kim et al. 2018). In addition to HATs, HDACs also affect plant regeneration. Inhibiting HDAC activity in Ara- Role of H4R3sme2 in plant regeneration bidopsis using the chemical inhibitor Trichostatin A (TSA) induced the transformation of hypocotyls into In addition to lysine methylation, histone arginine callus (Furuta et al. 2011) and induced somatic methylation is also involved in plant regeneration. embryogenesis in the absence of auxin (Wo´jcikowska Arabidopsis PROTEIN ARGININE METHYLTRANSFER- et al. 2018). Consistent with this observation, explants ASE 5 (PRMT5), which catalyzes the symmetric with a knocked-down expression of HISTONE DEACE- dimethylation at arginine 3 of histone H4 (H4R3sme2) TYLASE 19 (had19) showed enhanced embryogenic and RNA splicing factors, affects the transcription and responses. Speciﬁcally, HDA19 inhibits somatic protein levels of the cyclin-dependent kinase inhibitor embryogenesis by negatively regulating LEC1, LEC2, and KIP-RELATED PROTEIN 1 (KRP1) to participate in shoot BBM expression by reducing their acetylation levels regeneration (Liu et al. 2016a). PRMT5 deposits (Fig. 1B) (Moronczyk et al. 2022). However, when leaves H4R3sme2 on KRP1 and KRP2 to inhibit their tran- were used as the explant, TSA inhibited callus formation scription (Liu et al. 2016a). Furthermore, AtPRMT5 (Lee et al. 2016). Consistently, both hda9 and hd-tuins affects the alternative splicing of the E3 ubiquitin ligase protein1 (hdt1) mutants show reduced callus induction gene RELATED TO KPC1 (RKP), which produces an from leaves (Lee et al. 2016). abnormal RKP protein that cannot degrade KRP1 (Liu In rice, mature embryos are used as explants for et al. 2016a). KRP1 is up-regulated and KRP1 protein is callus formation. TSA treatment inhibited the formation stabilized in the atprmt5 mutant. Since KRP1 negatively of rice callus (Zhang et al. 2020). OsHDA710 decreases regulates cell division, cell division and shoot regener- the acetylation levels of the transcriptional repressor ation are inhibited in this mutant (Liu et al. 2016a). genes OsARF18 and OsARF22, thereby activating OsPLT1 and OsPLT2 to promote callus formation (Fig. 1B) Histone acetylation-regulated plant regeneration (Zhang et al. 2020). However, low concentrations of TSA promoted callus and shoot formation from mature The level of histone acetylation is regulated by histone wheat embryos, whereas high concentrations of TSA acetyltransferases (HATs) and histone deacetylases inhibited these processes (Bie et al. 2020). In addition, (HDACs) (Kumar et al. 2021). HATs activate gene treatment with the histone deacetylase inhibitor sodium expression by catalyzing the acetylation of histone butyrate enhanced regeneration in wheat (Bie et al. lysine tails, while HDACs remove acetyl groups to 2020). Therefore, HDACs play various roles in the repress gene expression. HATs and HDACs can add or regeneration of different explants in different species. remove acetylation at multiple lysine sites, including This variability is likely due to the promiscuous nature lysine 9 of histone H3 (H3K9), lysine 14 of histone H3 of histone acetylation modiﬁers, which modify multiple (H3K14), lysine 36 of histone H3 (H3K36), lysine 5 of lysine residues of different histones. histone H4 (H4K5), lysine 8 of histone H4 (H4K8), lysine 12 of histone H4 (H4K12), and lysine 16 of histone H4 The roles of histone variants in plant (H4K16) (Kumar et al. 2021). regeneration Histone acetylation levels change dynamically during various regeneration processes. During wound-induced In addition to histone modiﬁcation, histone variants callus formation, acetylation at lysine 9/14 of histone affect chromatin status and gene transcription (For- H3 (H3K9/14ac) and acetylation at lysine 27 of histone oozani et al. 2021). For instance, the histone variant The Author(s) 2023 aBIOTECH H2A.Z has dual functions in transcriptional activation with the deposition of H3K27me3 at the WUS promoter, and repression (Kumar 2018). In rice callus, H2A.Z is contributes to terminate ﬂoral meristem development enriched at the 5 ends of highly expressed genes, while in Arabidopsis (Sun et al. 2019). Thus, chromatin inactive gene bodies are covered by H2A.Z (Zhang et al. remodelers generally participate in the regulation of 2017a). The atypical H3 variant HISTONE THREE meristem identity in plant tissues. However, few reports RELATED 15 (H3.15) is involved in cell fate repro- have documented how manipulating chromatin remod- gramming during plant regeneration in Arabidopsis elers alters chromatin accessibility to inﬂuence plant (Yan et al. 2020). H3.15 lacks the K27 residue that is regeneration. In monocot wheat, the regeneration efﬁ- trimethylated, so its replacement would dilute ciency is generally low (Wang et al. 2017; Zhang et al. H3K27me3 levels (Yan et al. 2020). The H3.15-encoding 2018b). Co-expressing GROWTH REGULATING FACTOR gene HISTONE THREE RELATED 15 (HTR15) is gradually and 4-GRF INTERACTING FACTOR 1 (TaGRF4-TaGIF1) up-regulated by auxin signaling during callus formation greatly promoted regeneration in different wheat vari- induced by wounding or culture on CIM (Yan et al. eties (Debernardi et al. 2020). GIF recruits SWI/SNF 2020). During callus formation, H3.15 is deposited on chromatin remodeling complexes to its target genes to WOX11 and helps remove H3K27me3, thus promoting open the chromatin structure, thus allowing GRF4 to WOX11 expression and callus formation (Yan et al. regulate downstream gene expression (Kim 2019; Luo 2020). Consistently, the htr15 mutant has reduced callus and Palmgren 2021). Moreover, GIF1 functions together formation ability (Yan et al. 2020). with GRFs to recruit SWI/SNF chromatin remodeling complexes to shape inﬂorescence architecture in maize (Zea mays) (Li et al. 2022). CHROMATIN ACCESSIBILITY DYNAMICS ARE In Arabidopsis, auxin treatment altered the chromatin ASSOCIATED WITH THE CELL FATE TRANSITION accessibility of genes related to meristems and the cell DURING PLANT REGENERATION cycle, such as CYCLIN DEPENDENT KINASE B2;1 (CDKB2;1) and PLT7, to rewire the cell totipotency Chromatin accessibility dynamics are important for the network and drive somatic embryogenesis (Wang et al. regulation of gene expression and are in turn generally 2020). A comparison of immature embryos and seedling regulated by ATP-dependent chromatin remodeling explants revealed that open chromatin and the activated complexes (CRCs). Remodelers can alter the accessibil- expression of embryonic genes such as ABA INSENSI- ity of a speciﬁc genomic region to regulate DNA–histone TIVE 3 (ABI3), BBM, FUSCA 3 (FUS3), LEC1, and LEC2 are interactions by changing the position, occupancy, and required for somatic embryogenesis in Arabidopsis composition of nucleosomes using energy from ATP (Wang et al. 2020). Similarly, in wheat, the gain of hydrolysis. Remodelers are highly conserved. Four chromatin accessibility, along with the activation of key subfamilies of remodeler complexes have been charac- genes (such as TaBBM and TaWOX5) that mediate the terized in plants: CHROMODOMAIN HELICASE DNA cell fate transition, occurs during callus induction from BINDING (CHD), SWITCH DEFECTIVE/SUCROSE NON- immature embryos (Liu et al. 2022b). During shoot FERMENTING (SWI/SNF), IMITATION SWITCH (ISWI), regeneration from pluripotent callus in Arabidopsis, root and INOSITOL REQUIRING 80/SWI2/SNF2-RELATED 1 identity genes such as WOX5 gradually lose their chro- (INO80/SWR1) (Han et al. 2015; Ojolo et al. 2018). matin accessibility, while shoot identity genes such as Arabidopsis INO80 and the histone chaperones NAP1- PHYTOCHROME INTERACTING FACTOR 1 (PIF1) gain RELATED PROTEIN1 (NRP1) and NRP2 synergistically chromatin accessibility. Furthermore, the chromatin regulate inﬂorescence meristem (IM) size and RAM states of genes related to epidermal cell differentiation, activity by affecting the expression of auxin-related CK responses, and secondary metabolism gradually genes and preventing DNA damage to maintain chro- become more open (Wu et al. 2022). In rice, chromatin matin stability (Kang et al. 2019). PICKLE (PKL)isa is generally more open in the callus than in seedlings, CHD3 homolog in Arabidopsis that facilitates root with 58% more DNase I hypersensitive sites in the meristem activity (Aichinger et al. 2011) and maintains callus that are positively correlated with transcription root cell identity to limit embryogenesis by regulating (Zhang et al. 2012). During the process of protoplast the expression of the PRC2-encoding genes CLF and generation from leaf mesophyll cells in Arabidopsis, SWN (Aichinger et al. 2009). BRAHMA (BRM) is an SWI/ more accessible chromatin regions are created, leading SNF chromatin remodeling ATPase that maintains root to the random activation of WUS, which ultimately stem cell activity by directly targeting PIN genes (Yang promotes regeneration (Xu et al. 2021). et al. 2015). SPLAYED (SYD) is a SWI2/SNF2-like pro- Therefore, an accessible chromatin environment tein in the SNF2 subclass whose eviction, combined leads to higher totipotency, which is required for The Author(s) 2023 aBIOTECH regeneration. Chromatin accessibility dynamics are DNA methyltransferases affect shoot regeneration. associated with changes in the expression of key genes Compared to wild-type Arabidopsis, both the met1 single that drive the cell fate transition during different steps mutant and drm1 drm2 cmt3 (ddc) triple mutant show of plant regeneration. However, the general or speciﬁc enhanced competence for shoot regeneration (Shemer roles of individual chromatin remodelers in plant et al. 2015; Liu et al. 2018a; Shim et al. 2021). Fur- regeneration remain unclear. thermore, the ddc mutant regenerated shoots directly from roots on SIM without inducing callus formation (Shemer et al. 2015). During the two-step shoot DNA METHYLATION STATUS AFFECTS PLANT regeneration process, MET1 is highly expressed in the REGENERATION callus under the activation of ATE2FA (E2FA), and its expression is down-regulated on SIM (Liu et al. 2018a). In plants, DNA methylation occurs on cytosine, includ- MET1 maintains the DNA methylation of WUS and ing symmetrical CG methylation, CHG methylation, and inhibits WUS expression in the callus (Fig. 1C) (Liu et al. asymmetric CHH methylation (Law and Jacobsen 2010). 2018a). When MET1 was mutated, WUS, the CK signal- The establishment, maintenance, and removal of DNA ing genes ARR1 and ARR10, and the blue light receptor methylation marks are catalyzed by different enzymes gene CRYPTOCHROME 1 (CRY1) were activated to pro- (Law and Jacobsen 2010). DOMAINS REARRANGED mote shoot regeneration (Liu et al. 2018a; Shim et al. METHYLTRANSFERASE 2 (DRM2) catalyzes de novo 2021). Similarly, the up-regulation of WUS in the ddc methylation, whereas the maintenance of DNA methy- mutant resulted in the direct conversion of roots into lation requires different enzymes: CG methylation is shoots on SIM (Fig. 1C) (Shemer et al. 2015). However, maintained by DNA METHYLATRANSFERASE 1 (MET1, treatment with 5-azacytidine, which inhibits DNA also known as DMT1), CHG methylation is maintained methylation, has different effects on regeneration in by CHROMOMETHYLASE 3 (CMT3), and CHH methyla- different species. 5-azacytidine promoted the transfor- tion is maintained by DRM2 and CMT2 (Zhong et al. mation of peach leaves to callus (Zheng et al. 2022) but 2014). DNA demethylation is initially mediated by DNA inhibited callus formation in strawberry (Fragaria glycosidases, including DEMETER (DME), REPRESSOR ananassa) (Liu et al. 2022a). In addition, treatment with OF SILENCING 1 (ROS1), DEMETER-LIKE 2 (DML2), and 5-azacytidine enhanced somatic embryogenesis in Ara- DML3 (Law and Jacobsen 2010). bidopsis (Grzybkowska et al. 2018) but inhibited this Signiﬁcant changes in DNA methylation levels both process in rice (Hsu et al. 2018). These ﬁndings suggest globally and at local key genes occur during multiple that DNA methylation plays diverse roles in the regen- plant regeneration processes. Compared to leaves, glo- eration of different plant species. bal CHG methylation levels are higher and CHH methy- Plant regeneration competence is affected by the lation levels are lower in callus, which is consistent with explant’s age and variety, which are also related to DNA the up-regulation of CMT3 and down-regulation of methylation. The regeneration capacity of Boea hygro- CMT2 in callus (Shim et al. 2022). Cell proliferation- metrica leaves decreases during aging, which may be related genes, including PLT1, PLT2, ORIGIN RECOGNI- related to the high CHH methylation levels in mature TION COMPLEX 1 (ORC1), REPLICATION FACTORC 2 leaves (Sun et al. 2020). There are signiﬁcant differ- (RFC2), MITOTIC ARREST DEFICIENT 1 (MAD1), and ences in somatic embryogenesis competence between DISRUPTION OF MEIOTIC CONTROL 1 (DMC1), are the cotton (Gossypium hirsutum) cultivars Yuzao1 and hypomethylated in callus (Shim et al. 2022). The bind- Lumian1, which may be related to the level of CHH ing motifs of the circadian rhythm regulator genes methylation (Guo et al. 2020). Yuzao1 has a high CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) and LATE somatic embryo induction rate and CHH hypomethyla- ELONGATED HYPOCOTYL (LHY) are enriched in these tion, whereas Lumian1 has a low somatic embryo CHH-hypomethylated regions (Shim et al. 2022). Indeed, induction rate and CHH hypermethylation (Guo et al. CCA1 directly binds to the promoter of the cell division- 2020). Therefore, high DNA methylation levels reduce related gene ORC1 to inhibit its expression, which may the regeneration ability of plants. be related to the high CHH methylation levels of this promoter in leaves (Shim et al. 2022). During callus formation, CCA1 is inhibited and the CHH methylation MICRORNA LEVELS ARE ASSOCIATED WITH PLANT level of the ORC1 promoter decreases, thus releasing the REGENERATION CAPACITY expression of ORC1 and enhancing cell proliferation (Shim et al. 2022). miRNAs are a class of 21-nt non-coding small RNAs that reduce gene transcription by targeting mature mRNAs The Author(s) 2023 aBIOTECH (Axtell 2013). miRNAs such as miR156, miR160, 2016b). Furthermore, the transcriptional repressor miR167, miR319, and miR393 are involved in plant ARF10 binds directly to AuxRE in the promoter region regeneration via the direct or indirect regulation of of ARR15, which encodes a negative regulator of callus auxin and CK signaling genes. formation (Fig. 1D) (Liu et al. 2016b). Therefore, miR156 is involved in several age-related develop- miR160 inhibits regeneration by affecting both auxin mental processes (Xu et al. 2016; Guo et al. 2017). The and CK signaling pathways. In cotton, miR167 nega- shoot regeneration capacity of Arabidopsis and tobacco tively regulates somatic embryogenesis by targeting decreases with plant age, which can be compensated for ARF6 and ARF8 (Fig. 1D) (Arora et al. 2020). In plants by overexpressing MiR156 (Zhang et al. 2015). SQUA- overexpressing the miR167 target mimic MOSA PROMOTER BINDING PROTEIN-LIKE 9 (SPL9), (35S::MIM167), ARF6, ARF8, the auxin-responsive gene encoded by a gene targeted by miR156, directly binds to GRETCHEN HAGEN 3 (GH3), and the auxin transporter type-B ARR genes, including ARR1, ARR2, ARR10, and genes AUXIN RESISTANT 1 (AUX1), LIKE AUX1 3 (LAX3), ARR12, to impair CK responses (Fig. 1D) (Zhang et al. PIN1, and PIN2 were signiﬁcantly up-regulated, sug- 2015). High levels of miR156 inhibited SPL9 expression gesting that miR167 promotes somatic embryogenesis at the juvenile stage of Arabidopsis seedlings (Zhang by enhancing auxin signaling (Arora et al. 2020). In et al. 2015). After juvenile-to-adult transition, decreased addition to affecting ARF expression, miRNAs also affect miR156 levels led to the up-regulation of SPL9 and the the expression of auxin receptor-encoding genes, such inhibition of CK responses, thus weakening the capacity as TRANSPORT INHIBITOR RESPONSE 1 (TIR1) and for shoot regeneration (Zhang et al. 2015). The miR156- AUXIN SIGNALING F-BOX 3 (AFB3). TIR1 and AFB3 were SPL regulatory circuit plays a similar role in somatic up-regulated in a miR393 mutant, and the capacity for embryogenesis in citrus. For the majority of citrus cul- shoot regeneration and somatic embryogenesis was tivars, the callus gradually loses its embryogenesis higher in the mutant than in the wild type (Fig. 1D) capacity and fails to differentiate into shoots after long- (Wo´jcik and Gaj 2016; Wang et al. 2018). term culture (Long et al. 2018). miR156 levels are sig- niﬁcantly lower in non-embryonic than in embryonic callus, while its target genes CsSPL3 and CsSPL14 show CONCLUSIONS AND FUTURE PROSPECTS the opposite trend (Long et al. 2018). The expression levels of CsSPL3 and CsSPL14 are highly negatively Cell totipotency and cell fate determination are funda- correlated with somatic embryogenesis capacity in dif- mental research topics in biology. Plant regeneration ferent citrus varieties (Long et al. 2018). In the orange provides an excellent system for studying these topics. varieties ‘Anliu’, ‘Newhall’, ‘Valencia’, and ‘American’ sour Multi-step cell fate transitions occur during plant orange, which can undergo somatic embryogenesis, the regeneration, which are accompanied by chromatin expression levels of CsSPL3 and CsSPL14 are relatively landscape remodeling and transcriptome reprogram- low, while in varieties with weak competence for ming, particularly for cell identity genes such as WOX11, somatic embryogenesis, the expression levels of CsSPL3 WOX5, and WUS. Recent studies have improved our and CsSPL14 are high (Long et al. 2018). These obser- understanding of the functions of various epigenetic vations suggest that miR156-SPLs are involved in reg- regulators, such as histone modiﬁcation ‘writers’ and ulating age-dependent and variety-speciﬁc somatic ‘erasers’, chromatin remodelers, DNA methyltrans- embryogenesis in citrus. ferases, and miRNAs, in shaping plant regeneration by Similar to miR156, miR319 also promotes shoot altering the expression of cell identity genes. However, regeneration by affecting CK responses. The target many open questions remain. genes of miR319 are TCP3 and TCP4, encoding proteins Cell identity is associated with the accessibility of that directly activate ARR16, which encodes a negative speciﬁc portions of the genome, which is controlled by regulator of shoot regeneration (Fig. 1D) (Yang et al. interactions between genomic DNA and nucleosomes 2020). Loss-of-function of HUA ENHANCER 1 (HEN1), a containing various histones (Chen and Dent 2014). small RNA methyltransferase that stabilizes miR319, Altering DNA–histone interactions via chromatin modi- decreased miR319 levels, leading to the up-regulation of ﬁers would affect the transcriptional competency of TCP3 and TCP4, which in turn activated ARR16 and genes associated with speciﬁc regions of the genome inhibited shoot regeneration (Yang et al. 2020). (Klemm et al. 2019). Since cell identity frequently miRNAs also affect auxin signaling during plant switches during plant regeneration, multiple chromatin regeneration. miR160 targets ARF10 and inhibits auxin modiﬁers are required to broadly alter the accessibility signaling, which in turn inhibits callus and shoot of certain portions of the genome and speciﬁcally ﬁne- regeneration (Fig. 1D) (Qiao et al. 2012; Liu et al. tune the expression of key genes in coordination with The Author(s) 2023 aBIOTECH the activity of speciﬁc TFs. One challenging question is epigenetically modiﬁed targets. The diverse effects of how different chromatin modiﬁers function coopera- orthologous factors are likely related to the different tively to control regeneration. The speciﬁc expression or pre-existing cell identities in various explants or similar induction patterns of chromatin modiﬁers and their explants of different species. Special attention should be recruiters might differ for different targets or for the paid to characterizing the explant- or species-speciﬁc same targets but at different stages of regeneration. For reprogramming of epigenomics during regeneration. example, the methyltransferase ATXR2 of H3K36me3 Regeneration is widely used during the production of and demethylase JMJ30 of H3K9me3 both regulate genetically manipulated plants for agriculture. Whereas LBD16 and LBD19, but their regulation is interdepen- in Arabidopsis, transgenic or genome-edited plants can dent (Lee et al. 2018a). However, different chromatin be directly generated using the ﬂoral dip method modiﬁers might function together at the same loci. For (Clough and Bent 1998), major crops, including rice, instance, the removal of H3K27me3 and gain of chro- wheat, and maize, require long-term tissue culture (Hiei matin accessibility as well as increases in H3K4me3 at et al. 2014). The efﬁciency of genetic transformation speciﬁc gene clusters were detected during the early methods of crops has been improved by optimizing their callus induction step of wheat shoot regeneration from regeneration systems (Hayta et al. 2019) and by the immature embryos (Liu et al. 2022b). The detailed ectopic expression of genes encoding key regeneration mechanism that coordinates the activities of different factors such as WUS, BBM, and WOX5 (Lowe et al. 2016; chromatin modiﬁers remains to be elucidated. Wang et al. 2022). However, due to the diversity among Phytohormone signals, especially auxin and CK sig- species and explants, not all factors that function in nals, are essential during plant regeneration. Auxin and Arabidopsis regeneration can improve the efﬁciency of CK signals are transmitted to downstream target genes the genetic transformation of crops. Therefore, it is via ARF (Powers and Strader 2020) and type-B ARR (Li important to systematically study the regeneration et al. 2021) TFs, respectively. On the one hand, epige- processes of crops and to identify ‘novel’ factors that netic regulators can directly affect the expression of ARF can enhance the efﬁciency of crop regeneration. Several and ARR (Zhang et al. 2020) or targets of ARF and ARR recent studies have systematically analyzed gene by ‘‘hijacking’’ ARF and ARR (Lee et al. 2017, 2021)to expression and chromatin dynamics during the regen- deposit speciﬁc histone modiﬁcations that alter their eration process of rice (Zhao et al. 2020; Shim et al. transcriptional activity. On the other hand, certain epi- 2020), wheat (Liu et al. 2022b), and barley (Suo et al. genetic regulators are induced by auxin or CK signaling, 2021), providing valuable resources for mining key showing speciﬁc expression patterns during regenera- factors that enhance regeneration, such as TaDOF3.4 tion (Lee et al. 2018b, 2021). Therefore, additional and TaDOF5.6 in wheat (Liu et al. 2022b). However, studies are needed to explore the relationship between more in-depth analysis is still urgently needed to better plant hormonal signals and epigenetic regulators, par- understand the regeneration process and improve the ticularly to establish how auxin and CK inﬂuence epi- genetic transformation efﬁciency of crops. genetic regulators for global chromatin remodeling and Finally, the development of single-cell and spatial thus the cell fate transition. omics technologies (Xia et al. 2022) provides additional The mechanisms of epigenetic regulation of plant tools for tracing cells with regenerative origins in vari- regeneration, such as chromatin accessibility, ous explants and exploring the heterogeneity of callus in H3K27me3, and H3K4me3, are generally conserved the same generation or during transmission to the next among different species, indicating that knowledge generation (Mironova and Xu 2019;Xu etal. 2021; Zhai obtained studying model plants can be transferred to and Xu 2021). Such analyses will further enhance our less-studied species, such as crops with large and mechanistic understanding of plant regeneration, complex genomes [e.g., wheat, maize, and barley (Hor- thereby facilitating the development of advanced crop deum vulgare)]. However, epigenetic regulators show breeding tools. diverse, pleiotropic effects; the same factor may behave Acknowledgements We apologize to colleagues whose works differently or even in an opposite manner during dif- were not cited due to space limitations. This research was sup- ferent stages of the regeneration process. Moreover, ported by the Strategic Priority Research Program of the Chinese orthologous factors might exhibit various functions Academy of Sciences (XDA24010204), the National Key Research during the same stage of regeneration in different spe- and Development to Program of China (2021YFD1201500), and the National Natural Sciences Foundation of China (31970529) to cies or even in different explants of the same species. J.X. For these pleiotropic effects, in addition to epigenetic regulators per se, more attention needs to be paid to stage-speciﬁc recruiters that set the ‘speciﬁcity’ of The Author(s) 2023 aBIOTECH Data availability All data generated or analyzed during this Birnbaum KD, Alvarado AS (2008) Slicing across kingdoms: study are included in this published article and its supplementary regeneration in plants and animals. 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Publisher: Springer Journals
Copyright: Copyright © The Author(s) 2023
ISSN: 2096-6326
eISSN: 2662-1738
DOI: 10.1007/s42994-022-00093-2
Publisher site: See Article on Publisher Site

Abstract

aBIOTECH https://doi.org/10.1007/s42994-022-00093-2 aBIOTECH REVIEW Recent advances in understanding of the epigenetic regulation of plant regeneration 1,2& 1,2 1,2,3& Xuemei Liu , Kehui Zhu , Jun Xiao Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China CAS-JIC Centre of Excellence for Plant and Microbial Science (CEPAMS), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China Received: 27 October 2022 / Accepted: 27 December 2022 Abstract Ever since the concept of ‘‘plant cell totipotency’’ was ﬁrst proposed in the early twentieth century, plant regeneration has been a major focus of study. Regeneration-mediated organogenesis and genetic transformation are important topics in both basic research and modern agriculture. Recent studies in the model plant Arabidopsis thaliana and other species have expanded our understanding of the molecular regulation of plant regeneration. The hierarchy of transcriptional regulation driven by phytohormone signaling during regeneration is associated with changes in chromatin dynamics and DNA methylation. Here, we summarize how various aspects of epigenetic regulation, including histone modiﬁcations and variants, chromatin accessibility dynamics, DNA methylation, and microRNAs, modulate plant regeneration. As the mechanisms of epigenetic regulation are conserved in many plants, research in this ﬁeld has potential applications in boosting crop breeding, especially if coupled with emerging single-cell omics technologies. Keywords Plant regeneration, Epigenetic regulation, Arabidopsis, Crop breeding INTRODUCTION callus differentiation in tobacco (Nicotiana tabacum) (Skoog and Miller 1957), providing experimental tools From unicellular green algae to angiosperms, plants are and a conceptual framework for exploring the functions highly regenerative, meaning that new organs or whole of phytohormones and their interactions during regen- bodies can be rebuilt following injury (Ikeuchi et al. eration (Birnbaum and Alvarado 2008). Plant tissue 2016, 2019). Research on regeneration can be traced culture has been widely used in both basic research and back to Gottlieb Haberlandt’s description of totipotency agriculture and provides an excellent system for proposed in the early twentieth century (Haberlandt studying plant organogenesis and somatic embryogen- 2003; Krikorian and Berquam 2003; Thorpe 2007). In esis. Strategies that combine tissue culture and genome 1957, Skoog and Miller demonstrated that the ratio of editing technologies provide opportunities to geneti- exogenous auxin to cytokinin (CK) affects the fate of cally improve crops (Loyola-Vargas and Ochoa-Alejo 2018). Plant regeneration can be divided into two cate- Xuemei Liu and Kehui Zhu have contributed equally. gories: injury-induced regeneration and tissue culture- induced regeneration (Mathew and Prasad 2021). In the & Correspondence: xmliu@genetics.ac.cn (X. Liu), jxiao@genet- former, different regeneration processes occur ics.ac.cn (J. Xiao) The Author(s) 2023 aBIOTECH depending on the type of injury (Ikeuchi et al. 2016). and the expression of WOX5 and WOX7 is restricted to When the meristem is partially damaged, the plant will the stem cell niche (Hu and Xu 2016;Xu 2018; Jing et al. reconstruct the meristem, whereas when the meristem 2020). In addition, PLETHORA 1 (PLT1), PLT2, SCARE- is completely absent, the plant will grow axillary shoots CROW (SCR), and SHORT ROOT (SHR) are essential for or lateral roots. Some plant species, such as those in the quiescent center speciﬁcation and stem cell activity in Crassulaceae and Gesneriaceae families, can undergo de the RAM (Della Rovere et al. 2015; Shimotohno et al. novo organogenesis to form new shoots or roots from 2018). However, under the induction of CK in SIM, the cut sites (Ikeuchi et al. 2016). Other plants, however, callus differentiates into shoots. First, the expression of require tissue culture to regenerate the entire plant. CUP-SHAPED COTYLEDON1 (CUC1) and CUC2 in callus is Injury activates a range of genes, including cell cycle spatially reorganized to mark promeristem regions, and genes, genes involved in CK synthesis and responses, PIN-FORMED 1 (PIN1) is induced by CUCs to determine and genes encoding transcription factors (TFs) of the the future locations of shoot progenitors (Hibara et al. AP2/ERF family (Ikeuchi et al. 2017). WOUND INDUCED 2003; Daimon et al. 2003; Gordon et al. 2007; Shin et al. DEDIFFERENTIATION 1 (WIND1) is rapidly induced at 2020). Along with the up-regulation of PIN1, SHOOT the wounding site and promotes cell dedifferentiation to MERISTEMLESS (STM) is expressed in the promeristem form callus via type-B ARR (Iwase et al. 2011). Another to maintain shoot meristem activity (Gordon et al. 2007; gene in the AP2/ERF family, ETHYLENE RESPONSE Shin et al. 2020). In addition, type-B ARRs in the CK FACTOR 115 (ERF115), promotes reconstitution of the signaling pathway, including ARABIDOPSIS RESPONSE stem cell niche after root tip excision (Heyman et al. REGULATOR 1 (ARR1), ARR2, ARR10, and ARR12, 2016). directly bind to and activate WUSCHEL (WUS), which Tissue culture-induced regeneration can be divided directs the shoot apical meristem (SAM) formation into three types based on the culture system and program (Negin et al. 2017; Zhang et al. 2017b; Shin regeneration process used: de novo root regeneration, et al. 2020). de novo shoot regeneration, and somatic embryogenesis Unlike de novo root or shoot regeneration, somatic (Mathew and Prasad 2021). Both de novo root regen- embryogenesis leads to the formation of a bipolar eration and shoot regeneration are two-step processes. structure with an apical and basal pole. In Arabidopsis, The explant forms callus on an auxin-rich callus induc- somatic embryogenesis is often induced from 2,4- tion medium (CIM). The callus then differentiates into dichlorophenoxyacetic acid (2,4-D)-treated immature roots on root induction medium (RIM), which contains zygotic embryos at the bent cotyledon stage of devel- little or no auxin, or shoots on CK-rich shoot induction opment (Horstman et al. 2017). Ectopic expression of medium (SIM) (Lardon and Geelen 2020). Regardless of the embryo identity genes LEAFY COTYLEDON 1 (LEC1) the origin of the explant, the process of callus formation (Lotan et al. 1998) and LEC2 (Stone et al. 2001), the induced on CIM follows the root developmental path- meristem identity genes BABY BOOM (BBM) (Boutilier way (Sugimoto et al. 2010), and the identity of the callus et al. 2002) and WUS (Gaj 2004; Chatﬁeld et al. 2013), is similar to that of root primordia (Zhai and Xu 2021). and wound-induced WIND1 (Ikeuchi et al. 2013) indu- During this process, auxin signaling in Arabidopsis ces somatic embryogenesis. (Arabidopsis thaliana) ﬁrst activates WUSCHEL RELA- Plant cells undergo multiple rapid cell fate transitions TED HOMEOBOX 11 (WOX11) and WOX12, which during regeneration, which is accompanied by the transforms the regenerative pericycle or pericycle-like reprogramming of the transcriptome and chromatin cells of the explant into root founder cells (Atta et al. landscape. Cell identity genes, especially TF genes, are 2009; Liu et al. 2014; Sang et al. 2018;Xu 2018). Sub- induced by phytohormones to participate in plant sequently, in the continuous presence of auxin, WOX11/ regeneration (Sang et al. 2018; Ikeuchi et al. 2019; WOX12 activates the expression of WOX5, WOX7, LAT- Sugimoto et al. 2019; Mathew and Prasad 2021). The ERAL ORGAN BOUNDARIES-DOMAIN 16 (LBD16), and expression of these key TF genes is partially regulated LBD29, which in turn transform root founder cells into by various epigenetic regulators. In 2007, Crane and root primordium cells (Hu and Xu 2016;Xu 2018; Liu Gelvin reported that RNAi lines in which 24 genes et al. 2018b). Thus, callus is formed on CIM. encoding epigenetic regulators, including chromatin Subsequently, the ratio of auxin to CK determines the remodeling complexes, DNA methyltransferases, and direction of callus re-differentiation. On RIM, callus various histone modiﬁcation-related enzymes, had been resembling root primordia continues to undergo cell silenced showed altered genetic transformation efﬁ- division and differentiates into a well-organized root ciencies (Crane and Gelvin 2007). Further studies have apical meristem (RAM). During this process, LBD16 uncovered epigenetic dynamics during plant regenera- expression in the root meristem gradually decreases tion and highlighted the importance of the epigenetic The Author(s) 2023 aBIOTECH regulation of key TFs that drive the cell fate transition tissue culture-induced regeneration, and propose future during regeneration (Wang et al. 2020; Xu et al. 2021; directions for better understanding the different layers Wu et al. 2022). Here, we summarize recent advances in of epigenetic regulation of plant regeneration and their understanding the epigenetic regulation of the plant applications in crop breeding. regeneration process (Fig. 1, Table 1), with a focus on Fig. 1 Roles of epigenetic regulators in plant regeneration. Mechanisms of histone methylation (A), histone acetylation (B), DNA methylation (C), and miRNA (D) in regulating plant regeneration. The font color indicates the transcriptional status of the gene, with red representing transcriptional activation and blue representing transcriptional repression. The scissors represent the injury-induced regeneration. The arrows represent activation and the T-ended arrows represent inhibition The Author(s) 2023 aBIOTECH Table 1 Epigenetic regulators of plant regeneration Protein Protein ID Annotation Targets Roles in regeneration References name CLF AT2G23380 H3K27me3 SAW1, SAW2, ATH1, Inhibits somatic embryogenesis; He et al. (2012) methyltransferase TCP10 Promotes callus formation from leaves SWN AT4G02020 H3K27me3 SAW1, SAW2, ATH1, Inhibits somatic embryogenesis; He et al. (2012) methyltransferase TCP10 Promotes callus formation from leaves ATX4 AT4G27910 H3K4me3 ATH1, KANT4, Inhibits callus formation from Lee et al. (2019) methyltransferase SAW1, SAW2, leaves; Promotes shoot TCP10, YAB5 regeneration from callus LDL3 AT4G16310 H3K4me2 CIPK23, GLT1, Promotes shoot regeneration from Ishihara et al. (2019) demethylase UPL4, ARR12 callus ATXR2 AT3G21820 H3K36me3 LBD16, LBD29, Promotes callus formation from Lee et al. methyltransferase ARR5, ARR7 leaves; Inhibits shoot (2017, 2018b, 2021) regeneration from callus ASHR3 AT4G30860 H3K36me3 ARR1, PLT3, WIND3 Promotes wound-induced callus Lee et al. (2020) methyltransferase formation JMJ30 AT3G20810 H3K9me3 LBD16, LBD29 Promote callus formation from Lee et al. (2018a) demethylase leaves AtPRMT5 AT4G31120 H4R3sme2 KRP1 Promotes shoot regeneration from Liu et al. (2016a) methyltransferase callus HAG1 AT3G54610 histone WOX5, SCR, PLT1, Promotes wound-induced callus Kim et al. (2018), acetyltransferase PLT2 formation; Promotes shoot Rymen et al. (2019) regeneration from callus HAG3 AT5G50320 histone NA Promotes wound-induced callus Rymen et al. (2019) acetyltransferase formation HDA19 AT4G38130 histone LEC2 Inhibits somatic embryogenesis Moron´ czyk et al. deacetylases (2022) HDA9 AT3G44680 histone LBD17, LEC1 Inhibits callus formation from (Lee et al. 2016) deacetylases leaves HDT1 AT3G44750 histone BBM, WUS Inhibits callus formation from Lee et al. (2016) deacetylases leaves OsHDA710 Os02g0215200 histone OsARF18, OsARF22 Promote callus formation from Zhang et al. (2020) deacetylases embryos HTR15 AT5G12910 coding H3.15 WOX11 Promotes wound-induced callus Yan et al. (2020) formation; Promotes callus formation from hypocotyls INO80 AT3G57300 chromatin PIN1 Collaborates with histone Kang et al. (2019) remodeling chaperones NRP1/2 to regulate complexes IM and RAM activities PKL AT2G25170 chromatin LEC1, FUS3, ABI3, Facilitates root meristem activity; Aichinger et al. remodeling EMF2, CLF, SWN, Limits embryogenesis (2009, 2011) complexes AP3, AG, FLC BRM AT2G46020 chromatin Cyc81;1, CycB1;3, Maintains the root stem cell niche Yang et al. (2015) remodeling PIN1–4, PIN7 complexes CHR3 AT2G28290 chromatin WUS Maintains the ﬂoral meristem Sun et al. (2019) remodeling complexes MET1 AT5G49160 DNA WUS, ARR1, ARR10, Inhibits shoot regeneration from Liu et al. (2018a), Shim methyltransferase CRY1 callus et al. (2021) DRM1 AT5G15380 DNA WUS Inhibits shoot regeneration from Shemer et al. (2015) methyltransferase callus DRM2 AT5G14620 DNA WUS Inhibits shoot regeneration from Shemer et al. (2015) methyltransferase callus The Author(s) 2023 aBIOTECH Table 1 continued Protein Protein ID Annotation Targets Roles in regeneration References name CMT3 AT1G69770 DNA WUS Inhibits shoot regeneration from Shemer et al. (2015) methyltransferase callus miR156 microRNA SPL9 Promotes shoot regeneration; Zhang et al. (2015), Promotes somatic Long et al. (2018) embryogenesis miR319 microRNA TCP3, TCP4 Inhibits shoot regeneration Yang et al. (2020) miR160 microRNA ARF10 Inhibits callus formation; Inhibits Qiao et al. (2012), Liu shoot regeneration et al. (2016b) miR167 microRNA ARF6, ARF8 Inhibits somatic embryogenesis Arora et al. (2020) miR393 microRNA TIR1, AFB3 Inhibits shoot regeneration; Wo´jcik and Gaj (2016), Inhibits somatic embryogenesis Wang et al. (2018) LAYERS OF EPIGENETIC REGULATION histone has various effects on the transcriptional regu- OF TRANSCRIPTION lation of genes. In general, trimethylation at lysine 27 of histone H3 (H3K27me3) and trimethylation at lysine 9 Gene transcription is regulated at multiple levels. In of histone H3 (H3K9me3) negatively regulate tran- general, trans-acting TFs bind to cis-elements in their scription, whereas trimethylation at lysine 4 of histone target promoters to promote or inhibit gene transcrip- H3 (H3K4me3) and trimethylation at lysine 36 of his- tion. However, in the cellular environment, DNA is tone H3 (H3K36me3) are associated with transcrip- wrapped around histones and packaged into nucleo- tional activation (Xiao et al. 2016). Histone methylation somes, which limits the access of TFs. Transcription dynamics are regulated by ‘‘writers’’ that add methyl factors compete with histones and other chromatin- groups, such as histone lysine methyltransferase binding proteins to bind to DNA (Klemm et al. 2019). (HKMTs) and protein arginine methyltransferases Chromatin remodeling complexes can directly alter (PRMTs), and ‘‘erasers’’ that remove methyl group, such nucleosome composition and interactions, thereby as histone demethylases (HDMs) (Liu et al. 2010). affecting chromatin accessibility (Ojolo et al. 2018). Methylation or acetylation of histone H3 and H4 can H3K27me3 dynamics regulate plant regeneration affect the interactions between histones and DNA, resulting in loose or dense chromatin (Pﬂuger and In Arabidopsis, H3K27me3 is catalyzed by Polycomb Wagner 2007). DNA methylation is also involved in repressive complex 2 (PRC2), which consists of four transcriptional regulation. DNA methylation in promot- subunits. The catalytic subunit Enhancer of zeste ers inhibits gene transcription, whereas DNA methyla- homolog2 (EZH2) is encoded by three functionally tion in gene bodies is mostly associated with independent genes: CURLY LEAF (CLF), SWINGER constitutive expression (Zhang et al. 2018a). Post-tran- (SWN), and MEDEA (MEA). The spatial–temporal-speci- scriptional regulation, such as processes mediated by ﬁc expression of these genes leads to the functional microRNA (miRNA), can also affect gene expression diversiﬁcation of PRC2 (Bieluszewski et al. 2021). (Gibney and Nolan 2010). Instead of exhibiting normal plant architecture, the clf swn double mutant spontaneously forms a callus-like tissue that accumulates neutral lipids and occasionally REGULATION OF PLANT REGENERATION somatic embryo-like structures (Chanvivattana et al. VIA HISTONE MODIFICATIONS AND HISTONE 2004; Ikeuchi et al. 2015). Although auxin failed to VARIANTS induce somatic embryogenesis from wild-type shoots, this treatment induced somatic embryo formation from Histone methylation-regulated plant clf swn shoots (Mozgova´ et al. 2017). This observation regeneration suggests that the loss of function of PRC2 promotes somatic embryogenesis from vegetative tissues in Ara- The lysine or arginine residues of histone tails can be bidopsis. In rice (Oryza sativa), the H3K27me3 levels of modiﬁed by mono-, di- and tri-methylation, which OsWOX6, OsWOX9, OsWOX11, OsPLT3, OsPLT6, and affects transcription by altering the local chromatin OsPLT8 are signiﬁcantly lower in callus than in seedlings state. Methylation of residues at different positions of (Zhao et al. 2020). In peach (Prunus persica), during the The Author(s) 2023 aBIOTECH leaf-to-callus transition, the up-regulation of auxin-re- YAB5 to regain shoot identity (Fig. 1A) (Lee et al. 2019). lated genes PpPIN6 and AUXIN-INDUCED PROTEIN 13 Thus, ATX4-mediated H3K4me3 has dual functions in (PpIAA13) and the lateral root development-related callus induction and the re-differentiation of callus in genes PpLBD1, LATERAL ORGAN BOUNDARIES (PpLOB), Arabidopsis. By contrast, in crops such as wheat (Liu SHI RELATED SEQUENCE 1 (PpSRS1), and LATERAL et al. 2022b) and rice (Zhao et al. 2020), H3K4me3 ROOT PRIMORDIUM 1 (PpLRP1) is accompanied by a deposition increases during immature embryo- or seed- decrease in H3K27me3 levels (Zheng et al. 2022). Fur- induced callus formation, pointing to an opposite role thermore, treatment with the H3K27me3 demethylase for H3K4me3 in promoting callus formation in these inhibitor GSK-J4 signiﬁcantly reduced the rate of callus crops compared to Arabidopsis. This discrepancy might induction in peach (Zheng et al. 2022). In hexaploid be due to the different types of explants used for each wheat (Triticum aestivum), H3K27me3 deceases at species. auxin signaling genes and root meristem formation-re- In general, dimethylation at lysine 4 of histone H3 lated genes such as TaPIN1 and TaLBD17 during the late (H3K4me2) positively regulates gene expression in stage of callus formation from immature embryos (Liu animals (Barski et al. 2007) but is associated with gene et al. 2022b). Thus, the attenuation of H3K27me3 of repression in plants (Liu et al. 2019). LYSINE-SPECIFIC auxin signaling and meristematic-related genes could DEMETHYLASE 1-LIKE 3 (LDL3) accumulates and facilitate their activation and promote callus formation. speciﬁcally erases H3K4me2 marks on genes required By contrast, leaf tissue of the Arabidopsis clf swn mutant for the acquisition of shoot traits during callus forma- failed to form callus on CIM, because leaf identity genes, tion from root cells (Ishihara et al. 2019). Interestingly, such as SAWTOOTH 1 (SAW1), SAW2, ARABIDOPSIS LDL3-mediated removal of H3K4me2 does not imme- THALIANA HOMEOBOX GENE 1 (ATH1), and TCP diately activate target genes, but rather primes genes for DOMAIN PROTEIN 10 (TCP10), cannot be repressed subsequent activation during shoot induction on SIM without PRC2-mediated H3K27me3 deposition during (Ishihara et al. 2019). Accordingly, the competency of dedifferentiation and callus induction (Fig. 1A) (He et al. shoot regeneration is severely impaired in the ldl3 2012). In summary, PRC2-mediated H3K27me3 marks mutant due to its failure to eliminate H3K4me2 on meristematic genes in differentiated tissues to prevent shoot regeneration genes, such as CBL-INTERACTING callus formation, while it is also required to turn off PROTEIN KINASE 23 (CIPK23) and UBIQUITIN-PROTEIN tissue identity genes for the acquisition of pluripotency LIGASE 4 (UPL4) (Ishihara et al. 2019). and to facilitate callus formation. The status of H3K36me3 and H3K9me3 inﬂuences plant Altering H3K4me3 and H3K4me2 affects plant regeneration regeneration Signaling factors in the auxin and CK pathways interact During the leaf-to-callus transition in Arabidopsis, the with histone modiﬁers to regulate gene expression down-regulation of leaf identity genes is also regulated during plant regeneration. The H3K36me3 methyl- by the decrease in H3K4me3 levels. ARABIDOPSIS transferase gene ARABIDOPSIS TRITHORAX-RELATED 2 TRITHORAX 4 (ATX4) (Foroozani et al. 2021) catalyzes (ATXR2) (Lee et al. 2017) and the H3K9me3 demethy- the trimethylation of H3K4 and participates in de novo lase gene JUMONJI C DOMAIN-CONTAINING PROTEIN 30 shoot regeneration from leaf explants (Lee et al. 2019). (JMJ30) (Lee et al. 2018a) are constitutively up-regu- ATX4 is highly expressed in leaves and deposits lated upon callus induction on CIM. The auxin signaling H3K4me3 on the leaf identity genes ATH1, KNOTTED1- factors AUXIN RESPONSE FACTOR 7 (ARF7) and ARF19 LIKE HOMEOBOX GENE 4 (KNAT4), SAW1, SAW2, TCP10, interact with and recruit ATXR2 and JMJ30 to the pro- and YABBY 5 (YAB5) to maintain leaf cell identify. Upon moters of LBD16 and LBD29 and activate their expres- induction on CIM, the expression level of ATX4 decrea- sion to promote the dedifferentiation of leaf explants ses rapidly and remains low throughout callus induc- and callus formation (Fig. 1A) (Lee et al. 2017, 2018a). tion. As a result, the H3K4me3 and expression levels of Notably, both JMJ30-mediated decreases in H3K9me3 leaf identity genes decrease, which results in the loss of and ATXR2-mediated increases in H3K36me3 are leaf cell identity (Lee et al. 2019). Compared to the wild required for the activation of LBDs during the leaf-to- type, atx4 more readily generates callus from leaf tissue callus transition. ATXR2 also promotes root organo- (Lee et al. 2019). ATX4 also affects re-differentiation genesis on a phytohormone-free medium (Lee et al. from callus to shoot tissue. When callus is transferred to 2018b) and inhibits shoot regeneration on SIM (Lee SIM, ATX4 is temporarily up-regulated, and ATX4 re- et al. 2021). The atxr2 mutant shows enhanced shoot deposits H3K4me3 on ATH1, SAW1, SAW2, TCP10, and regeneration from the callus regardless of the origin of The Author(s) 2023 aBIOTECH the explant (Lee et al. 2021). ATXR2 interacts with type- H3 (H3K27ac) accumulate on genes that are up-regu- B ARR1 in the CK signaling pathway to deposit lated by wounding, such as WIND1, ERF113/RAP2.6L, H3K36me3 and activate ARR5 and ARR7 on SIM. ARR5 and LBD (Rymen et al. 2019). The histone acetyltrans- and ARR7 are type-A ARRs that inhibit WUS expression ferases HISTONE ACETYLTRANSFERASE OF THE GNAT and shoot formation (Lee et al. 2021). Therefore, auxin- FAMILY 1 (HAG1) and HAG3 promote callus formation inducible ATXR2 regulates CK signaling and precisely during wounding, as the callus formation rate is signif- controls WUS expression to prevent premature shoot icantly reduced in hag1 and hag3 mutants (Rymen et al. induction. Another H3K36me3 methyltransferase, 2019). HAG1 also promotes the transition of callus to ASH1-RELATED 3 (ASHR3), promotes wound-induced shoots. During de novo shoot regeneration, HAG1 cat- callus formation. Following wounding, ASHR3 is rapidly alyzes the acetylation of WOX5, SCR, PLT1, and PLT2 and activated and deposits H3K36me3 on ARR1, PLT3, and promotes their expression, allowing the callus to WIND3 to promote callus formation (Fig. 1A) (Lee et al. acquire competence for shoot regeneration (Fig. 1B) 2020). (Kim et al. 2018). In addition to HATs, HDACs also affect plant regeneration. Inhibiting HDAC activity in Ara- Role of H4R3sme2 in plant regeneration bidopsis using the chemical inhibitor Trichostatin A (TSA) induced the transformation of hypocotyls into In addition to lysine methylation, histone arginine callus (Furuta et al. 2011) and induced somatic methylation is also involved in plant regeneration. embryogenesis in the absence of auxin (Wo´jcikowska Arabidopsis PROTEIN ARGININE METHYLTRANSFER- et al. 2018). Consistent with this observation, explants ASE 5 (PRMT5), which catalyzes the symmetric with a knocked-down expression of HISTONE DEACE- dimethylation at arginine 3 of histone H4 (H4R3sme2) TYLASE 19 (had19) showed enhanced embryogenic and RNA splicing factors, affects the transcription and responses. Speciﬁcally, HDA19 inhibits somatic protein levels of the cyclin-dependent kinase inhibitor embryogenesis by negatively regulating LEC1, LEC2, and KIP-RELATED PROTEIN 1 (KRP1) to participate in shoot BBM expression by reducing their acetylation levels regeneration (Liu et al. 2016a). PRMT5 deposits (Fig. 1B) (Moronczyk et al. 2022). However, when leaves H4R3sme2 on KRP1 and KRP2 to inhibit their tran- were used as the explant, TSA inhibited callus formation scription (Liu et al. 2016a). Furthermore, AtPRMT5 (Lee et al. 2016). Consistently, both hda9 and hd-tuins affects the alternative splicing of the E3 ubiquitin ligase protein1 (hdt1) mutants show reduced callus induction gene RELATED TO KPC1 (RKP), which produces an from leaves (Lee et al. 2016). abnormal RKP protein that cannot degrade KRP1 (Liu In rice, mature embryos are used as explants for et al. 2016a). KRP1 is up-regulated and KRP1 protein is callus formation. TSA treatment inhibited the formation stabilized in the atprmt5 mutant. Since KRP1 negatively of rice callus (Zhang et al. 2020). OsHDA710 decreases regulates cell division, cell division and shoot regener- the acetylation levels of the transcriptional repressor ation are inhibited in this mutant (Liu et al. 2016a). genes OsARF18 and OsARF22, thereby activating OsPLT1 and OsPLT2 to promote callus formation (Fig. 1B) Histone acetylation-regulated plant regeneration (Zhang et al. 2020). However, low concentrations of TSA promoted callus and shoot formation from mature The level of histone acetylation is regulated by histone wheat embryos, whereas high concentrations of TSA acetyltransferases (HATs) and histone deacetylases inhibited these processes (Bie et al. 2020). In addition, (HDACs) (Kumar et al. 2021). HATs activate gene treatment with the histone deacetylase inhibitor sodium expression by catalyzing the acetylation of histone butyrate enhanced regeneration in wheat (Bie et al. lysine tails, while HDACs remove acetyl groups to 2020). Therefore, HDACs play various roles in the repress gene expression. HATs and HDACs can add or regeneration of different explants in different species. remove acetylation at multiple lysine sites, including This variability is likely due to the promiscuous nature lysine 9 of histone H3 (H3K9), lysine 14 of histone H3 of histone acetylation modiﬁers, which modify multiple (H3K14), lysine 36 of histone H3 (H3K36), lysine 5 of lysine residues of different histones. histone H4 (H4K5), lysine 8 of histone H4 (H4K8), lysine 12 of histone H4 (H4K12), and lysine 16 of histone H4 The roles of histone variants in plant (H4K16) (Kumar et al. 2021). regeneration Histone acetylation levels change dynamically during various regeneration processes. During wound-induced In addition to histone modiﬁcation, histone variants callus formation, acetylation at lysine 9/14 of histone affect chromatin status and gene transcription (For- H3 (H3K9/14ac) and acetylation at lysine 27 of histone oozani et al. 2021). For instance, the histone variant The Author(s) 2023 aBIOTECH H2A.Z has dual functions in transcriptional activation with the deposition of H3K27me3 at the WUS promoter, and repression (Kumar 2018). In rice callus, H2A.Z is contributes to terminate ﬂoral meristem development enriched at the 5 ends of highly expressed genes, while in Arabidopsis (Sun et al. 2019). Thus, chromatin inactive gene bodies are covered by H2A.Z (Zhang et al. remodelers generally participate in the regulation of 2017a). The atypical H3 variant HISTONE THREE meristem identity in plant tissues. However, few reports RELATED 15 (H3.15) is involved in cell fate repro- have documented how manipulating chromatin remod- gramming during plant regeneration in Arabidopsis elers alters chromatin accessibility to inﬂuence plant (Yan et al. 2020). H3.15 lacks the K27 residue that is regeneration. In monocot wheat, the regeneration efﬁ- trimethylated, so its replacement would dilute ciency is generally low (Wang et al. 2017; Zhang et al. H3K27me3 levels (Yan et al. 2020). The H3.15-encoding 2018b). Co-expressing GROWTH REGULATING FACTOR gene HISTONE THREE RELATED 15 (HTR15) is gradually and 4-GRF INTERACTING FACTOR 1 (TaGRF4-TaGIF1) up-regulated by auxin signaling during callus formation greatly promoted regeneration in different wheat vari- induced by wounding or culture on CIM (Yan et al. eties (Debernardi et al. 2020). GIF recruits SWI/SNF 2020). During callus formation, H3.15 is deposited on chromatin remodeling complexes to its target genes to WOX11 and helps remove H3K27me3, thus promoting open the chromatin structure, thus allowing GRF4 to WOX11 expression and callus formation (Yan et al. regulate downstream gene expression (Kim 2019; Luo 2020). Consistently, the htr15 mutant has reduced callus and Palmgren 2021). Moreover, GIF1 functions together formation ability (Yan et al. 2020). with GRFs to recruit SWI/SNF chromatin remodeling complexes to shape inﬂorescence architecture in maize (Zea mays) (Li et al. 2022). CHROMATIN ACCESSIBILITY DYNAMICS ARE In Arabidopsis, auxin treatment altered the chromatin ASSOCIATED WITH THE CELL FATE TRANSITION accessibility of genes related to meristems and the cell DURING PLANT REGENERATION cycle, such as CYCLIN DEPENDENT KINASE B2;1 (CDKB2;1) and PLT7, to rewire the cell totipotency Chromatin accessibility dynamics are important for the network and drive somatic embryogenesis (Wang et al. regulation of gene expression and are in turn generally 2020). A comparison of immature embryos and seedling regulated by ATP-dependent chromatin remodeling explants revealed that open chromatin and the activated complexes (CRCs). Remodelers can alter the accessibil- expression of embryonic genes such as ABA INSENSI- ity of a speciﬁc genomic region to regulate DNA–histone TIVE 3 (ABI3), BBM, FUSCA 3 (FUS3), LEC1, and LEC2 are interactions by changing the position, occupancy, and required for somatic embryogenesis in Arabidopsis composition of nucleosomes using energy from ATP (Wang et al. 2020). Similarly, in wheat, the gain of hydrolysis. Remodelers are highly conserved. Four chromatin accessibility, along with the activation of key subfamilies of remodeler complexes have been charac- genes (such as TaBBM and TaWOX5) that mediate the terized in plants: CHROMODOMAIN HELICASE DNA cell fate transition, occurs during callus induction from BINDING (CHD), SWITCH DEFECTIVE/SUCROSE NON- immature embryos (Liu et al. 2022b). During shoot FERMENTING (SWI/SNF), IMITATION SWITCH (ISWI), regeneration from pluripotent callus in Arabidopsis, root and INOSITOL REQUIRING 80/SWI2/SNF2-RELATED 1 identity genes such as WOX5 gradually lose their chro- (INO80/SWR1) (Han et al. 2015; Ojolo et al. 2018). matin accessibility, while shoot identity genes such as Arabidopsis INO80 and the histone chaperones NAP1- PHYTOCHROME INTERACTING FACTOR 1 (PIF1) gain RELATED PROTEIN1 (NRP1) and NRP2 synergistically chromatin accessibility. Furthermore, the chromatin regulate inﬂorescence meristem (IM) size and RAM states of genes related to epidermal cell differentiation, activity by affecting the expression of auxin-related CK responses, and secondary metabolism gradually genes and preventing DNA damage to maintain chro- become more open (Wu et al. 2022). In rice, chromatin matin stability (Kang et al. 2019). PICKLE (PKL)isa is generally more open in the callus than in seedlings, CHD3 homolog in Arabidopsis that facilitates root with 58% more DNase I hypersensitive sites in the meristem activity (Aichinger et al. 2011) and maintains callus that are positively correlated with transcription root cell identity to limit embryogenesis by regulating (Zhang et al. 2012). During the process of protoplast the expression of the PRC2-encoding genes CLF and generation from leaf mesophyll cells in Arabidopsis, SWN (Aichinger et al. 2009). BRAHMA (BRM) is an SWI/ more accessible chromatin regions are created, leading SNF chromatin remodeling ATPase that maintains root to the random activation of WUS, which ultimately stem cell activity by directly targeting PIN genes (Yang promotes regeneration (Xu et al. 2021). et al. 2015). SPLAYED (SYD) is a SWI2/SNF2-like pro- Therefore, an accessible chromatin environment tein in the SNF2 subclass whose eviction, combined leads to higher totipotency, which is required for The Author(s) 2023 aBIOTECH regeneration. Chromatin accessibility dynamics are DNA methyltransferases affect shoot regeneration. associated with changes in the expression of key genes Compared to wild-type Arabidopsis, both the met1 single that drive the cell fate transition during different steps mutant and drm1 drm2 cmt3 (ddc) triple mutant show of plant regeneration. However, the general or speciﬁc enhanced competence for shoot regeneration (Shemer roles of individual chromatin remodelers in plant et al. 2015; Liu et al. 2018a; Shim et al. 2021). Fur- regeneration remain unclear. thermore, the ddc mutant regenerated shoots directly from roots on SIM without inducing callus formation (Shemer et al. 2015). During the two-step shoot DNA METHYLATION STATUS AFFECTS PLANT regeneration process, MET1 is highly expressed in the REGENERATION callus under the activation of ATE2FA (E2FA), and its expression is down-regulated on SIM (Liu et al. 2018a). In plants, DNA methylation occurs on cytosine, includ- MET1 maintains the DNA methylation of WUS and ing symmetrical CG methylation, CHG methylation, and inhibits WUS expression in the callus (Fig. 1C) (Liu et al. asymmetric CHH methylation (Law and Jacobsen 2010). 2018a). When MET1 was mutated, WUS, the CK signal- The establishment, maintenance, and removal of DNA ing genes ARR1 and ARR10, and the blue light receptor methylation marks are catalyzed by different enzymes gene CRYPTOCHROME 1 (CRY1) were activated to pro- (Law and Jacobsen 2010). DOMAINS REARRANGED mote shoot regeneration (Liu et al. 2018a; Shim et al. METHYLTRANSFERASE 2 (DRM2) catalyzes de novo 2021). Similarly, the up-regulation of WUS in the ddc methylation, whereas the maintenance of DNA methy- mutant resulted in the direct conversion of roots into lation requires different enzymes: CG methylation is shoots on SIM (Fig. 1C) (Shemer et al. 2015). However, maintained by DNA METHYLATRANSFERASE 1 (MET1, treatment with 5-azacytidine, which inhibits DNA also known as DMT1), CHG methylation is maintained methylation, has different effects on regeneration in by CHROMOMETHYLASE 3 (CMT3), and CHH methyla- different species. 5-azacytidine promoted the transfor- tion is maintained by DRM2 and CMT2 (Zhong et al. mation of peach leaves to callus (Zheng et al. 2022) but 2014). DNA demethylation is initially mediated by DNA inhibited callus formation in strawberry (Fragaria glycosidases, including DEMETER (DME), REPRESSOR ananassa) (Liu et al. 2022a). In addition, treatment with OF SILENCING 1 (ROS1), DEMETER-LIKE 2 (DML2), and 5-azacytidine enhanced somatic embryogenesis in Ara- DML3 (Law and Jacobsen 2010). bidopsis (Grzybkowska et al. 2018) but inhibited this Signiﬁcant changes in DNA methylation levels both process in rice (Hsu et al. 2018). These ﬁndings suggest globally and at local key genes occur during multiple that DNA methylation plays diverse roles in the regen- plant regeneration processes. Compared to leaves, glo- eration of different plant species. bal CHG methylation levels are higher and CHH methy- Plant regeneration competence is affected by the lation levels are lower in callus, which is consistent with explant’s age and variety, which are also related to DNA the up-regulation of CMT3 and down-regulation of methylation. The regeneration capacity of Boea hygro- CMT2 in callus (Shim et al. 2022). Cell proliferation- metrica leaves decreases during aging, which may be related genes, including PLT1, PLT2, ORIGIN RECOGNI- related to the high CHH methylation levels in mature TION COMPLEX 1 (ORC1), REPLICATION FACTORC 2 leaves (Sun et al. 2020). There are signiﬁcant differ- (RFC2), MITOTIC ARREST DEFICIENT 1 (MAD1), and ences in somatic embryogenesis competence between DISRUPTION OF MEIOTIC CONTROL 1 (DMC1), are the cotton (Gossypium hirsutum) cultivars Yuzao1 and hypomethylated in callus (Shim et al. 2022). The bind- Lumian1, which may be related to the level of CHH ing motifs of the circadian rhythm regulator genes methylation (Guo et al. 2020). Yuzao1 has a high CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) and LATE somatic embryo induction rate and CHH hypomethyla- ELONGATED HYPOCOTYL (LHY) are enriched in these tion, whereas Lumian1 has a low somatic embryo CHH-hypomethylated regions (Shim et al. 2022). Indeed, induction rate and CHH hypermethylation (Guo et al. CCA1 directly binds to the promoter of the cell division- 2020). Therefore, high DNA methylation levels reduce related gene ORC1 to inhibit its expression, which may the regeneration ability of plants. be related to the high CHH methylation levels of this promoter in leaves (Shim et al. 2022). During callus formation, CCA1 is inhibited and the CHH methylation MICRORNA LEVELS ARE ASSOCIATED WITH PLANT level of the ORC1 promoter decreases, thus releasing the REGENERATION CAPACITY expression of ORC1 and enhancing cell proliferation (Shim et al. 2022). miRNAs are a class of 21-nt non-coding small RNAs that reduce gene transcription by targeting mature mRNAs The Author(s) 2023 aBIOTECH (Axtell 2013). miRNAs such as miR156, miR160, 2016b). Furthermore, the transcriptional repressor miR167, miR319, and miR393 are involved in plant ARF10 binds directly to AuxRE in the promoter region regeneration via the direct or indirect regulation of of ARR15, which encodes a negative regulator of callus auxin and CK signaling genes. formation (Fig. 1D) (Liu et al. 2016b). Therefore, miR156 is involved in several age-related develop- miR160 inhibits regeneration by affecting both auxin mental processes (Xu et al. 2016; Guo et al. 2017). The and CK signaling pathways. In cotton, miR167 nega- shoot regeneration capacity of Arabidopsis and tobacco tively regulates somatic embryogenesis by targeting decreases with plant age, which can be compensated for ARF6 and ARF8 (Fig. 1D) (Arora et al. 2020). In plants by overexpressing MiR156 (Zhang et al. 2015). SQUA- overexpressing the miR167 target mimic MOSA PROMOTER BINDING PROTEIN-LIKE 9 (SPL9), (35S::MIM167), ARF6, ARF8, the auxin-responsive gene encoded by a gene targeted by miR156, directly binds to GRETCHEN HAGEN 3 (GH3), and the auxin transporter type-B ARR genes, including ARR1, ARR2, ARR10, and genes AUXIN RESISTANT 1 (AUX1), LIKE AUX1 3 (LAX3), ARR12, to impair CK responses (Fig. 1D) (Zhang et al. PIN1, and PIN2 were signiﬁcantly up-regulated, sug- 2015). High levels of miR156 inhibited SPL9 expression gesting that miR167 promotes somatic embryogenesis at the juvenile stage of Arabidopsis seedlings (Zhang by enhancing auxin signaling (Arora et al. 2020). In et al. 2015). After juvenile-to-adult transition, decreased addition to affecting ARF expression, miRNAs also affect miR156 levels led to the up-regulation of SPL9 and the the expression of auxin receptor-encoding genes, such inhibition of CK responses, thus weakening the capacity as TRANSPORT INHIBITOR RESPONSE 1 (TIR1) and for shoot regeneration (Zhang et al. 2015). The miR156- AUXIN SIGNALING F-BOX 3 (AFB3). TIR1 and AFB3 were SPL regulatory circuit plays a similar role in somatic up-regulated in a miR393 mutant, and the capacity for embryogenesis in citrus. For the majority of citrus cul- shoot regeneration and somatic embryogenesis was tivars, the callus gradually loses its embryogenesis higher in the mutant than in the wild type (Fig. 1D) capacity and fails to differentiate into shoots after long- (Wo´jcik and Gaj 2016; Wang et al. 2018). term culture (Long et al. 2018). miR156 levels are sig- niﬁcantly lower in non-embryonic than in embryonic callus, while its target genes CsSPL3 and CsSPL14 show CONCLUSIONS AND FUTURE PROSPECTS the opposite trend (Long et al. 2018). The expression levels of CsSPL3 and CsSPL14 are highly negatively Cell totipotency and cell fate determination are funda- correlated with somatic embryogenesis capacity in dif- mental research topics in biology. Plant regeneration ferent citrus varieties (Long et al. 2018). In the orange provides an excellent system for studying these topics. varieties ‘Anliu’, ‘Newhall’, ‘Valencia’, and ‘American’ sour Multi-step cell fate transitions occur during plant orange, which can undergo somatic embryogenesis, the regeneration, which are accompanied by chromatin expression levels of CsSPL3 and CsSPL14 are relatively landscape remodeling and transcriptome reprogram- low, while in varieties with weak competence for ming, particularly for cell identity genes such as WOX11, somatic embryogenesis, the expression levels of CsSPL3 WOX5, and WUS. Recent studies have improved our and CsSPL14 are high (Long et al. 2018). These obser- understanding of the functions of various epigenetic vations suggest that miR156-SPLs are involved in reg- regulators, such as histone modiﬁcation ‘writers’ and ulating age-dependent and variety-speciﬁc somatic ‘erasers’, chromatin remodelers, DNA methyltrans- embryogenesis in citrus. ferases, and miRNAs, in shaping plant regeneration by Similar to miR156, miR319 also promotes shoot altering the expression of cell identity genes. However, regeneration by affecting CK responses. The target many open questions remain. genes of miR319 are TCP3 and TCP4, encoding proteins Cell identity is associated with the accessibility of that directly activate ARR16, which encodes a negative speciﬁc portions of the genome, which is controlled by regulator of shoot regeneration (Fig. 1D) (Yang et al. interactions between genomic DNA and nucleosomes 2020). Loss-of-function of HUA ENHANCER 1 (HEN1), a containing various histones (Chen and Dent 2014). small RNA methyltransferase that stabilizes miR319, Altering DNA–histone interactions via chromatin modi- decreased miR319 levels, leading to the up-regulation of ﬁers would affect the transcriptional competency of TCP3 and TCP4, which in turn activated ARR16 and genes associated with speciﬁc regions of the genome inhibited shoot regeneration (Yang et al. 2020). (Klemm et al. 2019). Since cell identity frequently miRNAs also affect auxin signaling during plant switches during plant regeneration, multiple chromatin regeneration. miR160 targets ARF10 and inhibits auxin modiﬁers are required to broadly alter the accessibility signaling, which in turn inhibits callus and shoot of certain portions of the genome and speciﬁcally ﬁne- regeneration (Fig. 1D) (Qiao et al. 2012; Liu et al. tune the expression of key genes in coordination with The Author(s) 2023 aBIOTECH the activity of speciﬁc TFs. One challenging question is epigenetically modiﬁed targets. The diverse effects of how different chromatin modiﬁers function coopera- orthologous factors are likely related to the different tively to control regeneration. The speciﬁc expression or pre-existing cell identities in various explants or similar induction patterns of chromatin modiﬁers and their explants of different species. Special attention should be recruiters might differ for different targets or for the paid to characterizing the explant- or species-speciﬁc same targets but at different stages of regeneration. For reprogramming of epigenomics during regeneration. example, the methyltransferase ATXR2 of H3K36me3 Regeneration is widely used during the production of and demethylase JMJ30 of H3K9me3 both regulate genetically manipulated plants for agriculture. Whereas LBD16 and LBD19, but their regulation is interdepen- in Arabidopsis, transgenic or genome-edited plants can dent (Lee et al. 2018a). However, different chromatin be directly generated using the ﬂoral dip method modiﬁers might function together at the same loci. For (Clough and Bent 1998), major crops, including rice, instance, the removal of H3K27me3 and gain of chro- wheat, and maize, require long-term tissue culture (Hiei matin accessibility as well as increases in H3K4me3 at et al. 2014). The efﬁciency of genetic transformation speciﬁc gene clusters were detected during the early methods of crops has been improved by optimizing their callus induction step of wheat shoot regeneration from regeneration systems (Hayta et al. 2019) and by the immature embryos (Liu et al. 2022b). The detailed ectopic expression of genes encoding key regeneration mechanism that coordinates the activities of different factors such as WUS, BBM, and WOX5 (Lowe et al. 2016; chromatin modiﬁers remains to be elucidated. Wang et al. 2022). However, due to the diversity among Phytohormone signals, especially auxin and CK sig- species and explants, not all factors that function in nals, are essential during plant regeneration. Auxin and Arabidopsis regeneration can improve the efﬁciency of CK signals are transmitted to downstream target genes the genetic transformation of crops. Therefore, it is via ARF (Powers and Strader 2020) and type-B ARR (Li important to systematically study the regeneration et al. 2021) TFs, respectively. On the one hand, epige- processes of crops and to identify ‘novel’ factors that netic regulators can directly affect the expression of ARF can enhance the efﬁciency of crop regeneration. Several and ARR (Zhang et al. 2020) or targets of ARF and ARR recent studies have systematically analyzed gene by ‘‘hijacking’’ ARF and ARR (Lee et al. 2017, 2021)to expression and chromatin dynamics during the regen- deposit speciﬁc histone modiﬁcations that alter their eration process of rice (Zhao et al. 2020; Shim et al. transcriptional activity. On the other hand, certain epi- 2020), wheat (Liu et al. 2022b), and barley (Suo et al. genetic regulators are induced by auxin or CK signaling, 2021), providing valuable resources for mining key showing speciﬁc expression patterns during regenera- factors that enhance regeneration, such as TaDOF3.4 tion (Lee et al. 2018b, 2021). Therefore, additional and TaDOF5.6 in wheat (Liu et al. 2022b). However, studies are needed to explore the relationship between more in-depth analysis is still urgently needed to better plant hormonal signals and epigenetic regulators, par- understand the regeneration process and improve the ticularly to establish how auxin and CK inﬂuence epi- genetic transformation efﬁciency of crops. genetic regulators for global chromatin remodeling and Finally, the development of single-cell and spatial thus the cell fate transition. omics technologies (Xia et al. 2022) provides additional The mechanisms of epigenetic regulation of plant tools for tracing cells with regenerative origins in vari- regeneration, such as chromatin accessibility, ous explants and exploring the heterogeneity of callus in H3K27me3, and H3K4me3, are generally conserved the same generation or during transmission to the next among different species, indicating that knowledge generation (Mironova and Xu 2019;Xu etal. 2021; Zhai obtained studying model plants can be transferred to and Xu 2021). Such analyses will further enhance our less-studied species, such as crops with large and mechanistic understanding of plant regeneration, complex genomes [e.g., wheat, maize, and barley (Hor- thereby facilitating the development of advanced crop deum vulgare)]. However, epigenetic regulators show breeding tools. diverse, pleiotropic effects; the same factor may behave Acknowledgements We apologize to colleagues whose works differently or even in an opposite manner during dif- were not cited due to space limitations. This research was sup- ferent stages of the regeneration process. Moreover, ported by the Strategic Priority Research Program of the Chinese orthologous factors might exhibit various functions Academy of Sciences (XDA24010204), the National Key Research during the same stage of regeneration in different spe- and Development to Program of China (2021YFD1201500), and the National Natural Sciences Foundation of China (31970529) to cies or even in different explants of the same species. J.X. For these pleiotropic effects, in addition to epigenetic regulators per se, more attention needs to be paid to stage-speciﬁc recruiters that set the ‘speciﬁcity’ of The Author(s) 2023 aBIOTECH Data availability All data generated or analyzed during this Birnbaum KD, Alvarado AS (2008) Slicing across kingdoms: study are included in this published article and its supplementary regeneration in plants and animals. 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aBIOTECH – Springer Journals

Published: Mar 1, 2023

Keywords: Plant regeneration; Epigenetic regulation; Arabidopsis; Crop breeding

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Recent advances in understanding of the epigenetic regulation of plant regeneration

Recent advances in understanding of the epigenetic regulation of plant regeneration

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Recent advances in understanding of the epigenetic regulation of plant regeneration

Recent advances in understanding of the epigenetic regulation of plant regeneration

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