Molecular regulation of tomato male reproductive development

Dandan Yang; Zhao Wang; Xiaozhen Huang; Cao Xu

doi:10.1007/s42994-022-00094-1

Molecular regulation of tomato male reproductive development

Yang, Dandan; Wang, Zhao; Huang, Xiaozhen; Xu, Cao 2023-03-01 00:00:00 aBIOTECH https://doi.org/10.1007/s42994-022-00094-1 aBIOTECH REVIEW Molecular regulation of tomato male reproductive development 1,2 1,3 1,2 1,2,3& Dandan Yang , Zhao Wang , Xiaozhen Huang , Cao Xu State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China CAS-JIC Centre of Excellence for Plant and Microbial Science, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China Received: 26 October 2022 / Accepted: 30 December 2022 Abstract The reproductive success of ﬂowering plants, which directly affects crop yield, is sensitive to envi- ronmental changes. A thorough understanding of how crop reproductive development adapts to climate changes is vital for ensuring global food security. In addition to being a high-value vegetable crop, tomato is also a model plant used for research on plant reproductive development. Tomato crops are cultivated under highly diverse climatic conditions worldwide. Targeted crosses of hybrid varieties have resulted in increased yields and abiotic stress resistance; however, tomato reproduction, especially male reproductive development, is sensitive to temperature ﬂuctuations, which can lead to aborted male gametophytes, with detrimental effects on fruit set. We herein review the cytological features as well as genetic and molecular pathways inﬂuencing tomato male reproductive organ development and responses to abiotic stress. We also compare the shared features among the associated regulatory mechanisms of tomato and other plants. Collectively, this review highlights the opportunities and challenges related to characterizing and exploiting genic male sterility in tomato hybrid breeding programs. Keywords Tomato, Climate change, Male, Reproductive development INTRODUCTION fertilization (Ke et al. 2021; Liu et al. 2021;Ma 2005). Fruits and seeds are two major components of human Flowering plants are among the most successful living diets; their production depends on reproductive devel- organisms at least partly because of their morphological opment-related activities (Gao et al. 2015;Lietal. diversity and ability to grow in various ecological 2018b). During plant reproduction, the male reproduc- niches, which is primarily because of reproductive tive organ (i.e., anther and ﬁlament) undergoes speciﬁc innovations (Chen et al. 2019; Ge et al. 2010). Repro- changes, including anther differentiation, functional ductive development is crucial for the maintenance of pollen production, and anther dehiscence, ultimately genetic diversity and involves complex processes during resulting in the release of mature pollen. The failure of diploid and haploid phases, including male and female any of these processes may lead to male sterility, limited organogenesis, meiosis, gametogenesis, pollination, and reproduction, and decreased crop production. Moreover, as sessile organisms, plants are highly susceptible to environmental factors, with the reproductive stage & Correspondence: caoxu@genetics.ac.cn (C. Xu) The Author(s) 2023 aBIOTECH (especially male reproduction-related processes) more produces specialized stamen cells and tissues (Goldberg sensitive to abiotic stress than the vegetative growth et al. 1993). More speciﬁcally, the L1 layer cells develop stage (Zhang et al. 2021). An exposure to abiotic stress into the epidermis and stomium, whereas the L3 layer may impair anther and pollen development, resulting in cells produce the connective, vascular bundle, and cir- male sterility and low crop yields. Clarifying plant cular cell clusters adjacent to the stomium. Meanwhile, responses to abiotic stress during the male gameto- the periclinal division of the L2 layer cells results in the phytic phase is critical for enhancing crop productivity. initiation of the anther primordia, which subsequently Additionally, male-sterile varieties are valuable resour- differentiate into the archesporial cells and generate the ces, because they may be used to produce hybrids. inner microspore mother cells and the outer parietal Modulating male reproductive development may facili- cell layer (outer to inner layers: endothecium, middle tate the efﬁcient use of biotechnology-based male layer, and tapetum). The tapetum is a single layer of sterility for the selective breeding and commercial metabolically active cells and most obvious anther cell development of hybrid lines (Chen and Liu 2014). layer. Of the two basic tapetum types, the amoeboid Tomato, which is one of the most important veg- tapetum extends into the locule encasing the micro- etable crops, is cultivated worldwide. Although tomato spore to provide the microspore with required materials plants can grow under various climatic conditions, their (e.g., in Arum species or Cichorium intybus), whereas the reproductive development, especially male reproductive secretory tapetum, which is more common among development, is severely impeded by abiotic stresses, plants (e.g., Arabidopsis thaliana, rice, and tomato), resulting in decreased yields and relatively low fruit provides nutrients through the liquid in the locule that quality (Gerszberg and Hnatuszko-Konka 2017). Many bathes the developing microspore (Pacini 2010). The studies conducted over the last few decades to maintain tapetum is a nutritive somatic tissue accompanying with or increase tomato production focused on anther and the pollen development by providing nutrition to pollen development. We herein review the cytological microspores, enzymes for microspores release, precur- and morphological changes associated with tomato sors for pollen wall formation and small RNAs to reg- male organ development, the molecular and genetic ulate germline cells (Ma et al. 2021; Santiago et al. 2019; pathways inﬂuencing tomato male reproduction-related Shi et al. 2015; Wang et al. 2018; Yao et al. 2022). activities, and the general mechanisms by which abiotic Programmed cell death (PCD)-triggered tapetal cells stresses can inhibit tomato male reproductive develop- degradation plays a vital role in nutrition supply, which ment. We also describe experimental strategies useful often occurs synchronously with post-meiotic micro- for enhancing tomato male reproductive development spore development and is tightly controlled by inte- under abiotic stress conditions. gration of internal and external signals (Parish et al. 2012). In tomato, tapetum degradation is initiated before the tetrad stage and is completed at the bicellular TOMATO MALE REPRODUCTIVE DEVELOPMENT pollen stage (Fig. 1). Recent research on tomato revealed that premature or delayed tapetum degenera- After producing 8–10 leaves, the shoot apical vegetative tion usually results in male sterility (Pan et al. 2021;Yan meristem of tomato plants transforms into an inﬂores- et al. 2020; Yang et al. 2021). cence meristem, which ultimately forms a lateral In addition to the outer layer of parietal cells, the monochasial inﬂorescence that includes 6–10 ﬂowers inner microspore mother cells also contribute to pollen (Huang et al. 2018; Park et al. 2012). Tomato ﬂowers development, which is one of the most basic biological typically consist of ﬁve sepals and ﬁve petals that are processes related to plant sexual reproduction. Pollen arranged in an alternating pattern. The ﬁve anti-sepa- development involves the following two major stages: lous stamens are fused together to form a cone around microsporogenesis (i.e., differentiation of sporogenous the style inside of the petals. On the basis of morpho- cells and meiosis) and microgametogenesis (i.e., post- logical and cytological characteristics, the tomato ﬂoral meiotic microspore development) (Go´mez et al. 2015). developmental process has been divided into 20 stages In tomato, microspore mother cells have a relatively (Brukhin et al. 2003). The stamen primordia are large nucleus and are surrounded by parietal cells at detectable at stage 3 after the sepal and petal primordia ﬂoral developmental stage 7 (Fig. 1). The sporogenous have been initiated, but before the initiation of carpel cells undergo meiosis at stage 9 and produce a callose- primordia, and initially form as a whorl of small bumps encased tetrad. At stage 10, the callose is hydrolyzed by at a speciﬁc site on the surface of the ﬂoral meristem b-1, 3-glucanase secreted from tapetal cells, resulting in (Brukhin et al. 2003). During these processes, the divi- the release of free microspores from the tetrad (Fig. 1) sion of the ﬂoral meristem L1, L2, and L3 layers (Brukhin et al. 2003; Pan et al. 2021). The released The Author(s) 2023 aBIOTECH Fig. 1 Schematic overview of tomato anther and pollen development. SlPIF4-SlDYT1-SlTDF1-SlAMS-SlMS1, ROS, and sugar pathways affect tomato tapetum development. SlRECQ4, SlFANCM, and SlGIGL1 participate in tomato meiosis. SlPIF3, SlKRPs, and IAA regulate pollen mitosis I. The dashed line indicates a putative role or relationship microspores continue to develop using nutrients from mutant, with vestigial stamens adhering to the carpels the degenerated tapetal cells. The formation of vacuoles (Bishop 1954). The tomato spl-like mutant is indistin- within microspores is accompanied by the migration of guishable from wild-type tomato in terms of vegetative the nucleus to one side of the cell (Fig. 1). Vacuolated development, but its anthers have a ﬁlamentous struc- microspores undergo an asymmetrical mitotic division ture and do not produce pollen, leading to male sterility to generate pollen grains that comprise two cells with (Rojas-Gracia et al. 2017). In Arabidopsis, the tran- differing characteristics. The larger vegetative cell has a scription factors sporocyteless/nozzle (spl/nzz) mutants dispersed nucleus and more cytoplasm, whereas the were initially identiﬁed as sterile mutants, which dis- smaller generative cell, which is enclosed entirely by the played failure of male and female gametophyte forma- vegetative cell, contains condensed chromatin and rel- tion (Schiefthaler et al. 1999; Yang et al. 1999). atively little cytoplasm (Fig. 1). As pollen grains mature, Additionally, SPL/NZZ had also been demonstrated as a a break in the stomium that leads to pollen release is transcriptional repressor during Arabidopsis ovule due to the degeneration of the tapetum and the rein- development as the C-terminal end of SPL/NZZ contains forcement of the exothecium. In tomato, the generative a typical EAR motif (ERF-associated amphiphilic cell of the released pollen grains divides into two sperm repression), a well-characterized repression domain cells during pollen mitosis II (PMII) in the pollen tube (Ohta et al. 2001; Wei et al. 2015). A MADS-box tran- that grows through the pistil. In contrast, in Arabidopsis scription factor AGAMOUS (AG) that deﬁnes stamens and rice, PMII occurs in the anther sacs (Borg et al. and carpels regulates microsporogenesis and pollen 2009; McCormick 2004). formation by activating the expression of SPL/NZZ (Ito et al. 2004; Schiefthaler et al. 1999; Yang et al. 1999). Earlier research conﬁrmed that SlDEFICIENS (SlDEF) is GENES INVOLVED IN TOMATO MALE REPRODUCTIVE necessary for the normal development of petal and DEVELOPMENT stamen characteristics, while tomato MADS-box 6 (SlTM6) modulates stamen morphology (Cao et al. Male reproductive development involves multiple 2019; De Martino et al. 2006). In tomato, stigma stages, with abnormalities at any stage potentially exsertion has been observed in functional male-sterile leading to male sterility (i.e., structural, functional, or mutants (i.e., positional sterility). A recent investigation sporogenous male-sterile mutants) (Kaul 2012). In indicated that stigma exsertion is due to different genes tomato, structural male-sterile mutants usually have in diverse tomato genotypes, including genes at several extremely deformed stamens unable to produce pollen. loci associated with long styles (e.g., se2.1, StyleD1, and In contrast, functional male-sterile mutants form viable sty 8.1) (Cheng et al. 2021). A mutation to a polygalac- pollen grains that cannot reach the stigma because of a turonase-encoding gene, ps-2, results in non-dehiscent protruding style or indehiscent anthers. Stamenless (sl) anthers in tomato (Gorguet et al. 2009). Some mutants was the ﬁrst veriﬁed structural male-sterile tomato with abnormal jasmonic acid and ethylene metabolism The Author(s) 2023 aBIOTECH exhibit impaired tomato anther dehiscence (Schubert conserved roles in regulating tapetal development in et al. 2019). tomato. Most tomato male-sterile mutants exhibit sporoge- As mentioned above, during the establishment and nous male sterility. Accordingly, they have morphologi- speciﬁcation of the anther cell layers, sporogenous cells cally normal ﬂowers that produce little or no viable encased in the tapetum are generated from archesporial pollen (Gorman et al. 1997). The tomato male-sterile cells. The sporogenous cells then undergo a conserved mutant ms10 resulting from a spontaneous mutation cell division necessary for eukaryotic sexual reproduc- shows degenerating microspores with enlarged vac- tion (i.e., meiosis), which leads to the generation of uoles during meiosis. A gene mapping analysis revealed haploid microspores. Meiosis comprises the following that Ms10 encodes a bHLH transcription factor and is ﬁve key stages: meiotic entry, recombination initiation, homologous to the Arabidopsis gene DYSFUNCTIONAL chromosome synapsis, resolution of recombination TAPETUM 1 (DYT1) (Jeong et al. 2014). This gene intermediates, and the second meiotic division (Ma encodes a transcription factor that functions down- 2005). Defective meiosis generally prevents the pro- stream of SPL/NZZ, but is one of the earliest tapetal duction of viable pollen grains. Genes involved in development-related genes to be activated after another meiosis were identiﬁed in Arabidopsis and other crops cells are initiated (Zhang et al. 2006). Additionally, DYT1 following analyses of mutants that are sterile or less regulates the expression of many tapetal genes, such as fertile than normal (Wang et al. 2021). Both Topoiso- TAPETAL DEVELOPMENT1 (TDF1) and ABORTED merase3a (TOP3a) and RecQ-mediated instability 1 MICROSPORES (AMS), the latter of which encodes a (RMI1), which are components of the RTR (RecQ/Top3/ master regulator of tapetal development involved in the Rmi1) complex, are crucial for meiosis; mutations to the synthesis of lipidic and phenolic components essential corresponding Arabidopsis genes result in meiotic for pollen wall patterning and ﬂavonoid production (Gu defects and sterility. Analyses of tomato plants indicated et al. 2014; Sorensen et al. 2003; Zhu et al. 2008). In the the mutation in the top3a mutant is lethal to embryos, ms10 mutant, the expression levels of Soly- whereas the mutation in the rmi1 mutant does not c03g113530, Solyc08g062780, and Solyc04g008420, cause abnormalities in somatic DNA repair or meiosis which are homologs of AtTDF1, AtAMS, and MALE (Xing et al. 2012). Meiotic crossovers generate genetic STERILITY1 (AtMS1), respectively, are downregulated. diversity but improper crossover frequency can disrupt In addition to ms10 , the tomato male sterility 32 meiosis and cause pollen sterile in many plant species. A (ms32) mutant fails to undergo meiosis; its mutated group of genes that exert the function for limiting locus was mapped to a putative gene (Solyc01g081100) meiotic recombination have been identiﬁed in Ara- homologous to the Arabidopsis bHLH89/91 gene (Liu bidopsis, including Fanconi anemia of complementation et al. 2019). Moreover, the Solyc01g081100 expression group M (FANCM), Recombinant Escherichia coli ATP- level is downregulated in ms10 , suggesting that dependent DNA helicase (RECQ) and AAAATPase FIDGE- bHLH89/91 function downstream of DYT1 in tomato. In TIN-LIKE-1 (FIGL1). In contrast to the fact that loss of Arabidopsis, AMS has been reported to interact with function of these genes individually increases the bHLH89/91 to regulate the expression of MYB80, which crossover frequency and has little effect on fertility in promotes the sporopollenin synthesis for pollen wall Arabidopsis (Mieulet et al. 2018), the rice Osﬁgl1 mutant formation (Ferguson et al. 2017; Lou et al. 2014; Wang gives rise to aborted pollen, which may result from et al. 2018; Xiong et al. 2016; Zhang et al. 2007). The abnormal chromosome behavior during meiosis (Zhang rice bHLH protein UNDEVELOPED TAPETUM (OsUDT1), et al. 2017). Similarly, the tomato Slﬁgl1 mutant is also a putative homolog of AtDYT1, acts after initiation of the completely sterile, supporting the essential role of tapetum in an analogous manner to AtDYT1 (Jung et al. SlFIGL1 for fertility (Mieulet et al. 2018). To date, a few 2005). Moreover, a couple of important genes that are studies have been conducted on meiosis in tomato, essential for tapetum development have been cloned which has resulted in the identiﬁcation and characteri- from male-sterile rice mutants, including TAPETUM zation of several genes involved in meiosis. For example, DEGENERATION RETADATION (TDR) and OsMYB80, silencing MUTS-HOMOLOG 2 (MSH2), which encodes a which are homologs of AtAMS and AtMYB80, respec- protein that recognizes and repairs errors in DNA tively (Han et al. 2021; Pan et al. 2020; Phan et al. 2011; sequences, disrupts tomato male meiosis where half of Wilson and Zhang 2009). The functional similarity the meiocytes stalled at the zygotene stage or combined shared among these genes in both dicots and monocots to form diploid tetrads, which substantially inhibits suggest that the DYT1-TDF1-AMS-MYB80 transcrip- normal pollen formation (Sarma et al. 2018; Wang et al. tional cascade might also play an essential and 2021). The Author(s) 2023 aBIOTECH The post-meiosis pollen developmental stage is pathways are involved in pollen mitosis in tomato. microgametogenesis, in which microspores form pollen Recent research demonstrated that SlSWEET5b facili- grains via cellular mitosis. This process depends on the tates tomato pollen mitosis and maturation by mediat- asymmetrical division of the microspore during pollen ing the transport of apoplasmic hexose into developing mitosis I (PMI), which is essential for establishing male pollen cells (Ko et al. 2022), while SlMAPK20 is neces- germ cells (McCormick 2004). During mitosis in somatic sary for the uninucleate-to-binucleate transition of cell, the division site is marked by a circumferential tomato pollen cells, because it regulates anther sugar band of microtubules, called the preprophase band. metabolism (Chen et al. 2018). The molecular and reg- Although no obvious preprophase bands are observed ulatory mechanisms underlying the effects of sugar-re- in microspores before division, the migration of micro- lated signaling pathways on pollen mitosis will need to spore nuclear is sensitive to colchicine, suggesting the be more precisely characterized in future studies. involvement of a microtubule system (Twell et al. 1998). Thus, the ﬁne mapping of male sterility-related genes Compelling evidence comes from studies of the orchid and the identiﬁcation of genes associated with genic Phalaenopsis, in which a specialized generative pole male sterility in tomato have deepened our under- microtubule system appears at the future generative cell standing of the molecular basis of male reproductive pole prior to nuclear migration (Brown and Lemmon development and may increase the utility of biotech- 1991). In Arabidopsis, mutations in microtubule-related nology-based male sterility systems in hybrid breeding genes impact asymmetrical division of microspores and programs. cause abnormal male germline formation, ultimately lead to male sterility, such as gemini pollen1 (gem1), two-in-one (tio) and kinesin- 12A/ 12B (Liu and Qu ADAPTIVE RESPONSES OF TOMATO MALE 2008; Twell 2011). Given that the microtubule system REPRODUCTIVE DEVELOPMENT TO ABIOTIC plays an important role in directing and maintaining STRESSES nuclear migration, one can expect that it might act in response to cellular signals or polarity determinants Extreme environmental stresses, including excessive within the cytoplasm. However, the underlying mecha- heat, cold, and drought, adversely affect male fertility in nisms are still unclear so far. Mutations to cell-cycle ﬂowering plants and cause substantial crop yield losses. regulators in Arabidopsis can impair the progression of For example, high-temperature stress can negatively pollen mitosis with lethal consequences for gameto- affect male reproductive structures and processes (e.g., phytes (Liu and Qu 2008; Liu et al. 2008; Takatsuka stigma exsertion or anther indehiscence), leading to et al. 2015). Loss-of-function of genes related to decreased pollen dispersal and fruit set in tomato (Pan microtubules or cell-cycle regulators in tomato also et al. 2019; Sato et al. 2002). In most plants, the pro- directly affects the asymmetrical division of pollen cells cesses from meiosis to PMI are especially vulnerable to (Yang et al. 2022). In addition, some intracellular abiotic stress. When pollen development reaches the metabolites help regulate pollen mitosis. For example, in meiotic stage, the tapetal cells are highly metabolically Arabidopsis, the auxin ﬂow in anthers affects pollen active, with 20- to 40-fold increases in mitochondrial development by regulating PMI (Feng et al. 2006). activities (Parish et al. 2012). There is increasing evi- Additionally, the mutations in the yuc2yuc6 double dence of the link between abiotic stress-induced male mutant result in arrested PMI and a lack of viable pollen sterility and tapetal dysfunction (Go´mez et al. 2015). (Yao et al. 2018). Thus, auxin is vital for asymmetrical Excessive heat is not the only temperature-related pollen cell division. In tomato, a mutation to SlPIF3 stress that can decrease crop yields. Even mild tem- prevents the production of viable pollen grains because perature ﬂuctuations have induced grain yield losses of of the associated arrested PMI. Compared with wild- approximately 10%, 5.5%, and 3.8% per 1 C increase type tomato plants, the Slpif3 mutant has a substantially in rice, wheat, and maize, respectively (Lobell et al. lower anther auxin content and abnormal microtubule- 2011; Peng et al. 2004; Tashiro and Wardlaw 1989). An and cell-cycle-related gene expression levels (Yang et al. exposure to heat stress can induce male sterility in 2022). The application of exogenous auxin downregu- Arabidopsis, rice, wheat, and tomato by impairing lates the expression of cyclin kinase inhibitor genes tapetum differentiation and microsporogenesis, acti- (SlKRP2 and SlKRP4), while also partially rescuing the vating tapetal PCD prematurely, and inhibiting the pollen viability of the Slpif3 mutant, suggesting that dehiscence of anthers (Parish et al. 2012). At the auxin regulates tomato PMI by modulating the expres- molecular level, heat stress induces oxidative damage, sion of genes related to microtubules and the cell cycle. prevents proteins from folding correctly, and disturbs Furthermore, sugar metabolism-associated signaling hormone homeostasis (Fig. 2A). In response to heat The Author(s) 2023 aBIOTECH Fig. 2 Regulatory pathway of the tomato anther and pollen development in response to abiotic stress. A High-temperature (HT) stress induces ROS production and the tomato tapetal PCD process, leading to male sterility. An exposure to HT stress also increases the HSF and UPR expression levels, thereby enhancing the ability of tomato anthers and pollen grains to tolerate heat stress. B Low-temperature (LT) stress leads to abnormal anther m A levels and increased ABA contents in tomato, which adversely affects sugar metabolism by decreasing CWIN expression levels and delaying tapetal PCD degradation, ultimately resulting in male sterility. Moreover, LT stress enhances the production of SlPIF4, which interacts with SlDYT1 and induces SlTDF1 expression, which leads to delayed tapetal PCD. Drought inhibits tapetal degradation through the ABA and IAA signaling pathways. Upward and downward pointing red arrows indicate signiﬁcant increases and decreases, respectively. The dashed line indicates a putative role or relationship stress, mitochondria increase the production of reactive that produce antioxidant enzymes that eliminate oxygen species (ROS) via enhanced aerobic metabolism excessive ROS in cells (Parish et al. 2012). Increases in and cause oxidative damage and cell death, with crucial ROS levels reportedly induce the production of detoxi- effects on tapetal PCD in Arabidopsis, rice, and tomato ﬁcation-related enzymes in wheat pollen (Kumar et al. (Parish et al. 2012; Zhang et al. 2021). A recent study 2014). Additionally, increasing ROS contents can showed that loss-of-function mutations to DWARF upregulate the expression of HEAT SHOCK TRANSCRIP- (DWF) and BRASSINAZOLE-RESISTANT1 (BZR1) alter the TION FACTOR A1 (HsfA1), which substantially activates timing of ROS production and delay tapetal PCD in the expression of heat responsive genes. In Arabidopsis tomato (Yan et al. 2020). These ﬁndings provide evi- and tomato hsfa1 mutants, the expression levels of dence that ROS homeostasis in anthers contributes to many HS-responsive genes are lower than normal, the regulation of tapetal cell degeneration. Heat stress resulting in vegetative tissues with HS-insensitive phe- promotes the production of protein disulﬁde isomerase notypes (Mishra et al. 2002; Yoshida et al. 2011). Many 9 (PDI9), which affects nascent and misfolded proteins HSF and HSP genes are highly expressed in tomato in the endoplasmic reticulum; a mutation to the corre- microsporocytes and microspores, and their expression sponding gene decreases pollen viability at high tem- levels may be further increased by heat stress (Cha- peratures (Feldeverd et al. 2020). Plants rely on diverse turvedi et al. 2013). For example, SlHsfA2 regulates the mechanisms to withstand heat stress, including the expression of several HS-responsive genes and main- production of antioxidants and ROS scavengers as well tains pollen viability in plants exposed to heat stress as the induction of heat shock transcription factors during meiosis in the microspore stage, suggestive of (HSFs) and heat shock proteins (HSPs) (Chaturvedi et al. the importance of HsfA2 for pollen thermotolerance 2013). Heat stress may also activate a regulatory loop in (Fragkostefanakis et al. 2016). The contribution of which accumulating ROS modulate signaling cascades AtHsfA5 to pollen thermotolerance was revealed in an The Author(s) 2023 aBIOTECH earlier study in which the pollen abortion rate was negative correlation between the anther ABA content relatively high for the Athsfa5 mutant because of and pollen fertility (Oliver et al. 2007). In tomato, an defective HS responses (Renˇ a´k et al. 2014). Phytohor- exposure to cold stress signiﬁcantly increases anther mone signaling pathways typically mediate plant ABA levels, but the expression of SlCWIN7, which is responses to abiotic stress. Excessive heat causes the homologous to the rice gene OsINV4, signiﬁcantly abscisic acid (ABA) level to increase in rice anthers, decreases, suggesting that low temperatures disrupt whereas the IAA and GA contents decrease, leading to a anther sugar metabolism, which leads to pollen sterility decrease in pollen fertility (Zhang et al. 2021). The (Yang et al. 2021). Reversible epigenetic modiﬁcations application of exogenous auxin can reverse the male typically occur in developing plants in response to sterility of barley plants exposed to high temperatures, environmental stress. At low temperatures, N6-methy- demonstrating that auxin defection was an essential ladenosine (m A) levels decrease in tomato anthers, factor responsible for the heat stress-induced male which results in the altered transcription of many pollen sterility (Sakata et al. 2010). Notably, the AUXIN development-related genes (Yang et al. 2021). These RESPONSE FACTOR17 (ARF17) was reported to directly ﬁndings suggest m A may inﬂuence tomato pollen regulate the expression of CALLOSE SYNTHASE5 (CalS5), development under cold conditions. Similar to cold the key gene for callose biosynthesis. The miR160 reg- stress, drought conditions can interfere with tapetal ulated expression of ARF17 is also required for its development by preventing or delaying the induction of function during anthers development in Arabidopsis PCD in developing tomato pollen grains (Lamin-Samu (Wang et al. 2017; Yang et al. 2013). Both ABA and GA et al. 2021). Analyses of transcription levels and hor- are candidate signaling molecules that affect tapetal mone metabolism showed that in tomato anthers, development by regulating carbohydrate availability in drought stress upregulates the expression of genes the tapetum and microspores under abiotic stresses related to tapetum development and ABA homeostasis, (Zhang et al. 2021). whereas it has the opposite effect on the expression of Cold stress is another prevalent abiotic factor affect- sugar metabolism-associated genes, leading to ing the growth and development of plants, especially increased ABA levels and decreased soluble sugar con- subtropical vegetable crops. In Arabidopsis and rice, tents, which is consistent with what has been reported cold stress usually delays or inhibits tapetum regener- for other crops (Ji et al. 2011; Oliver et al. 2007). These ation by disrupting tapetal PCD, resulting in infertile results imply that in tomato, drought stress has detri- pollen (Zhang et al. 2021). In developing tomato anthers mental effects on the metabolism of carbohydrates and and pollen grains, PCD-triggered tapetum degradation is hormones. The molecular mechanisms linking tapetal initiated during the tetrad stage, intensiﬁes from the development and anther sugar and ABA homeostasis early-to-late uninucleate stage, and is undetectable at remain unclear. Future research will need to elucidate the binucleate pollen stage. Cold stress in tomato leads the cold- and/or drought-induced changes to these to irregular hypertrophy and tapetum vacuolation mechanisms that lead to tapetal dysfunction. because of delayed PCD, which subsequently leads to pollen abortion (Fig. 2B) (Pan et al. 2021; Yang et al. 2021). In contrast, pollen grains develop normally in the CONCLUSIONS AND FUTURE PERSPECTIVES tomato Slpif4 mutant under cold stress conditions because the inhibited activation of SlTDF1 makes the Increases in the global population as well as climate tapetum relatively insensitive to low temperatures changes are major issues that must be addressed to (Fig. 2B) (Pan et al. 2021). The inhibition of invertase maintain agricultural production and food security. In may be associated with tapetal hypertrophy and vac- addition to increasing crop yields, minimizing abiotic uolation. For example, during male gametogenesis in stress-induced production losses is a major objective rice, low-temperature stress causes ABA to accumulate, among plant researchers. Thoroughly characterizing the which may suppress the expression of the tapetum- mechanism regulating male fertility and identifying speciﬁc cell wall invertase gene OsINV4 and the novel stress resistance genes associated with male monosaccharide transporter genes OsMST8 and reproductive development may enable the generation of OsMST7, leading to abnormalities in anther sugar stress-resistant germplasm resources suitable for metabolism and male sterility (Oliver et al. 2005). biotechnology-based crop breeding. Research regarding Abscisic acid has vital functions related to plant devel- reproductive stress tolerance has continued to progress opment and mediates responses to abiotic stress. because multiple strategies have been applied. For Increased ABA levels improve plant abiotic stress tol- example, protein phase separations have been revealed erance during the vegetative growth stage, but there is a to contribute to plant adaptive responses to cellular pH The Author(s) 2023 aBIOTECH Science Foundation of China (U1903202) and Major Research Plan changes, temperature ﬂuctuations, and oxidative stress. of National Natural Science Foundation of China (31991183) to In Arabidopsis, a prion-like domain in ELF3 functions as C.X. and China National Postdoctoral Program for Innovative a putative thermo-sensor to undergo protein phase Talents (BX20220336) to D.Y. transition that results in the formation of liquid droplets in response to increasing temperatures (Jung et al. Data availability Data sharing not applicable to this article as no datasets were generated or analysed during the current study. 2020). The oxidation in the tomato shoot apical meris- tem triggers protein phase separations that enable TMF Declarations to bind to the promoter of the ﬂoral identity gene ANANTHA to repress its expression (Huang et al. 2021). Conﬂict of interest The authors declare that they have no com- peting interests. The reversible protein phase separation promoted by changing internal and external conditions is responsible Open Access This article is licensed under a Creative Commons for the ﬂexibility with which plants respond to global Attribution 4.0 International License, which permits use, sharing, climate changes; this may represent a new abiotic stress adaptation, distribution and reproduction in any medium or for- mat, as long as you give appropriate credit to the original mechanism inﬂuenced by plant developmental cues, author(s) and the source, provide a link to the Creative Commons especially those related to reproductive development. licence, and indicate if changes were made. The images or other Stress resistance is typically a complex and polygenic third party material in this article are included in the article’s trait. Developing novel plant lines with desirable traits Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s through polygenic editing is a considerable challenge. Creative Commons licence and your intended use is not permitted There are numerous extant wild relatives of tomato that by statutory regulation or exceeds the permitted use, you will are highly tolerant to various stresses. Therefore, the de need to obtain permission directly from the copyright holder. To novo domestication of wild tomato species has been view a copy of this licence, visit http://creativecommons.org/ proposed as a viable alternative for creating climate- licenses/by/4.0/. smart crops via genome engineering (Li et al. 2018a). 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Publisher: Springer Journals
Copyright: Copyright © The Author(s) 2023
ISSN: 2096-6326
eISSN: 2662-1738
DOI: 10.1007/s42994-022-00094-1
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Abstract

aBIOTECH https://doi.org/10.1007/s42994-022-00094-1 aBIOTECH REVIEW Molecular regulation of tomato male reproductive development 1,2 1,3 1,2 1,2,3& Dandan Yang , Zhao Wang , Xiaozhen Huang , Cao Xu State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China CAS-JIC Centre of Excellence for Plant and Microbial Science, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China Received: 26 October 2022 / Accepted: 30 December 2022 Abstract The reproductive success of ﬂowering plants, which directly affects crop yield, is sensitive to envi- ronmental changes. A thorough understanding of how crop reproductive development adapts to climate changes is vital for ensuring global food security. In addition to being a high-value vegetable crop, tomato is also a model plant used for research on plant reproductive development. Tomato crops are cultivated under highly diverse climatic conditions worldwide. Targeted crosses of hybrid varieties have resulted in increased yields and abiotic stress resistance; however, tomato reproduction, especially male reproductive development, is sensitive to temperature ﬂuctuations, which can lead to aborted male gametophytes, with detrimental effects on fruit set. We herein review the cytological features as well as genetic and molecular pathways inﬂuencing tomato male reproductive organ development and responses to abiotic stress. We also compare the shared features among the associated regulatory mechanisms of tomato and other plants. Collectively, this review highlights the opportunities and challenges related to characterizing and exploiting genic male sterility in tomato hybrid breeding programs. Keywords Tomato, Climate change, Male, Reproductive development INTRODUCTION fertilization (Ke et al. 2021; Liu et al. 2021;Ma 2005). Fruits and seeds are two major components of human Flowering plants are among the most successful living diets; their production depends on reproductive devel- organisms at least partly because of their morphological opment-related activities (Gao et al. 2015;Lietal. diversity and ability to grow in various ecological 2018b). During plant reproduction, the male reproduc- niches, which is primarily because of reproductive tive organ (i.e., anther and ﬁlament) undergoes speciﬁc innovations (Chen et al. 2019; Ge et al. 2010). Repro- changes, including anther differentiation, functional ductive development is crucial for the maintenance of pollen production, and anther dehiscence, ultimately genetic diversity and involves complex processes during resulting in the release of mature pollen. The failure of diploid and haploid phases, including male and female any of these processes may lead to male sterility, limited organogenesis, meiosis, gametogenesis, pollination, and reproduction, and decreased crop production. Moreover, as sessile organisms, plants are highly susceptible to environmental factors, with the reproductive stage & Correspondence: caoxu@genetics.ac.cn (C. Xu) The Author(s) 2023 aBIOTECH (especially male reproduction-related processes) more produces specialized stamen cells and tissues (Goldberg sensitive to abiotic stress than the vegetative growth et al. 1993). More speciﬁcally, the L1 layer cells develop stage (Zhang et al. 2021). An exposure to abiotic stress into the epidermis and stomium, whereas the L3 layer may impair anther and pollen development, resulting in cells produce the connective, vascular bundle, and cir- male sterility and low crop yields. Clarifying plant cular cell clusters adjacent to the stomium. Meanwhile, responses to abiotic stress during the male gameto- the periclinal division of the L2 layer cells results in the phytic phase is critical for enhancing crop productivity. initiation of the anther primordia, which subsequently Additionally, male-sterile varieties are valuable resour- differentiate into the archesporial cells and generate the ces, because they may be used to produce hybrids. inner microspore mother cells and the outer parietal Modulating male reproductive development may facili- cell layer (outer to inner layers: endothecium, middle tate the efﬁcient use of biotechnology-based male layer, and tapetum). The tapetum is a single layer of sterility for the selective breeding and commercial metabolically active cells and most obvious anther cell development of hybrid lines (Chen and Liu 2014). layer. Of the two basic tapetum types, the amoeboid Tomato, which is one of the most important veg- tapetum extends into the locule encasing the micro- etable crops, is cultivated worldwide. Although tomato spore to provide the microspore with required materials plants can grow under various climatic conditions, their (e.g., in Arum species or Cichorium intybus), whereas the reproductive development, especially male reproductive secretory tapetum, which is more common among development, is severely impeded by abiotic stresses, plants (e.g., Arabidopsis thaliana, rice, and tomato), resulting in decreased yields and relatively low fruit provides nutrients through the liquid in the locule that quality (Gerszberg and Hnatuszko-Konka 2017). Many bathes the developing microspore (Pacini 2010). The studies conducted over the last few decades to maintain tapetum is a nutritive somatic tissue accompanying with or increase tomato production focused on anther and the pollen development by providing nutrition to pollen development. We herein review the cytological microspores, enzymes for microspores release, precur- and morphological changes associated with tomato sors for pollen wall formation and small RNAs to reg- male organ development, the molecular and genetic ulate germline cells (Ma et al. 2021; Santiago et al. 2019; pathways inﬂuencing tomato male reproduction-related Shi et al. 2015; Wang et al. 2018; Yao et al. 2022). activities, and the general mechanisms by which abiotic Programmed cell death (PCD)-triggered tapetal cells stresses can inhibit tomato male reproductive develop- degradation plays a vital role in nutrition supply, which ment. We also describe experimental strategies useful often occurs synchronously with post-meiotic micro- for enhancing tomato male reproductive development spore development and is tightly controlled by inte- under abiotic stress conditions. gration of internal and external signals (Parish et al. 2012). In tomato, tapetum degradation is initiated before the tetrad stage and is completed at the bicellular TOMATO MALE REPRODUCTIVE DEVELOPMENT pollen stage (Fig. 1). Recent research on tomato revealed that premature or delayed tapetum degenera- After producing 8–10 leaves, the shoot apical vegetative tion usually results in male sterility (Pan et al. 2021;Yan meristem of tomato plants transforms into an inﬂores- et al. 2020; Yang et al. 2021). cence meristem, which ultimately forms a lateral In addition to the outer layer of parietal cells, the monochasial inﬂorescence that includes 6–10 ﬂowers inner microspore mother cells also contribute to pollen (Huang et al. 2018; Park et al. 2012). Tomato ﬂowers development, which is one of the most basic biological typically consist of ﬁve sepals and ﬁve petals that are processes related to plant sexual reproduction. Pollen arranged in an alternating pattern. The ﬁve anti-sepa- development involves the following two major stages: lous stamens are fused together to form a cone around microsporogenesis (i.e., differentiation of sporogenous the style inside of the petals. On the basis of morpho- cells and meiosis) and microgametogenesis (i.e., post- logical and cytological characteristics, the tomato ﬂoral meiotic microspore development) (Go´mez et al. 2015). developmental process has been divided into 20 stages In tomato, microspore mother cells have a relatively (Brukhin et al. 2003). The stamen primordia are large nucleus and are surrounded by parietal cells at detectable at stage 3 after the sepal and petal primordia ﬂoral developmental stage 7 (Fig. 1). The sporogenous have been initiated, but before the initiation of carpel cells undergo meiosis at stage 9 and produce a callose- primordia, and initially form as a whorl of small bumps encased tetrad. At stage 10, the callose is hydrolyzed by at a speciﬁc site on the surface of the ﬂoral meristem b-1, 3-glucanase secreted from tapetal cells, resulting in (Brukhin et al. 2003). During these processes, the divi- the release of free microspores from the tetrad (Fig. 1) sion of the ﬂoral meristem L1, L2, and L3 layers (Brukhin et al. 2003; Pan et al. 2021). The released The Author(s) 2023 aBIOTECH Fig. 1 Schematic overview of tomato anther and pollen development. SlPIF4-SlDYT1-SlTDF1-SlAMS-SlMS1, ROS, and sugar pathways affect tomato tapetum development. SlRECQ4, SlFANCM, and SlGIGL1 participate in tomato meiosis. SlPIF3, SlKRPs, and IAA regulate pollen mitosis I. The dashed line indicates a putative role or relationship microspores continue to develop using nutrients from mutant, with vestigial stamens adhering to the carpels the degenerated tapetal cells. The formation of vacuoles (Bishop 1954). The tomato spl-like mutant is indistin- within microspores is accompanied by the migration of guishable from wild-type tomato in terms of vegetative the nucleus to one side of the cell (Fig. 1). Vacuolated development, but its anthers have a ﬁlamentous struc- microspores undergo an asymmetrical mitotic division ture and do not produce pollen, leading to male sterility to generate pollen grains that comprise two cells with (Rojas-Gracia et al. 2017). In Arabidopsis, the tran- differing characteristics. The larger vegetative cell has a scription factors sporocyteless/nozzle (spl/nzz) mutants dispersed nucleus and more cytoplasm, whereas the were initially identiﬁed as sterile mutants, which dis- smaller generative cell, which is enclosed entirely by the played failure of male and female gametophyte forma- vegetative cell, contains condensed chromatin and rel- tion (Schiefthaler et al. 1999; Yang et al. 1999). atively little cytoplasm (Fig. 1). As pollen grains mature, Additionally, SPL/NZZ had also been demonstrated as a a break in the stomium that leads to pollen release is transcriptional repressor during Arabidopsis ovule due to the degeneration of the tapetum and the rein- development as the C-terminal end of SPL/NZZ contains forcement of the exothecium. In tomato, the generative a typical EAR motif (ERF-associated amphiphilic cell of the released pollen grains divides into two sperm repression), a well-characterized repression domain cells during pollen mitosis II (PMII) in the pollen tube (Ohta et al. 2001; Wei et al. 2015). A MADS-box tran- that grows through the pistil. In contrast, in Arabidopsis scription factor AGAMOUS (AG) that deﬁnes stamens and rice, PMII occurs in the anther sacs (Borg et al. and carpels regulates microsporogenesis and pollen 2009; McCormick 2004). formation by activating the expression of SPL/NZZ (Ito et al. 2004; Schiefthaler et al. 1999; Yang et al. 1999). Earlier research conﬁrmed that SlDEFICIENS (SlDEF) is GENES INVOLVED IN TOMATO MALE REPRODUCTIVE necessary for the normal development of petal and DEVELOPMENT stamen characteristics, while tomato MADS-box 6 (SlTM6) modulates stamen morphology (Cao et al. Male reproductive development involves multiple 2019; De Martino et al. 2006). In tomato, stigma stages, with abnormalities at any stage potentially exsertion has been observed in functional male-sterile leading to male sterility (i.e., structural, functional, or mutants (i.e., positional sterility). A recent investigation sporogenous male-sterile mutants) (Kaul 2012). In indicated that stigma exsertion is due to different genes tomato, structural male-sterile mutants usually have in diverse tomato genotypes, including genes at several extremely deformed stamens unable to produce pollen. loci associated with long styles (e.g., se2.1, StyleD1, and In contrast, functional male-sterile mutants form viable sty 8.1) (Cheng et al. 2021). A mutation to a polygalac- pollen grains that cannot reach the stigma because of a turonase-encoding gene, ps-2, results in non-dehiscent protruding style or indehiscent anthers. Stamenless (sl) anthers in tomato (Gorguet et al. 2009). Some mutants was the ﬁrst veriﬁed structural male-sterile tomato with abnormal jasmonic acid and ethylene metabolism The Author(s) 2023 aBIOTECH exhibit impaired tomato anther dehiscence (Schubert conserved roles in regulating tapetal development in et al. 2019). tomato. Most tomato male-sterile mutants exhibit sporoge- As mentioned above, during the establishment and nous male sterility. Accordingly, they have morphologi- speciﬁcation of the anther cell layers, sporogenous cells cally normal ﬂowers that produce little or no viable encased in the tapetum are generated from archesporial pollen (Gorman et al. 1997). The tomato male-sterile cells. The sporogenous cells then undergo a conserved mutant ms10 resulting from a spontaneous mutation cell division necessary for eukaryotic sexual reproduc- shows degenerating microspores with enlarged vac- tion (i.e., meiosis), which leads to the generation of uoles during meiosis. A gene mapping analysis revealed haploid microspores. Meiosis comprises the following that Ms10 encodes a bHLH transcription factor and is ﬁve key stages: meiotic entry, recombination initiation, homologous to the Arabidopsis gene DYSFUNCTIONAL chromosome synapsis, resolution of recombination TAPETUM 1 (DYT1) (Jeong et al. 2014). This gene intermediates, and the second meiotic division (Ma encodes a transcription factor that functions down- 2005). Defective meiosis generally prevents the pro- stream of SPL/NZZ, but is one of the earliest tapetal duction of viable pollen grains. Genes involved in development-related genes to be activated after another meiosis were identiﬁed in Arabidopsis and other crops cells are initiated (Zhang et al. 2006). Additionally, DYT1 following analyses of mutants that are sterile or less regulates the expression of many tapetal genes, such as fertile than normal (Wang et al. 2021). Both Topoiso- TAPETAL DEVELOPMENT1 (TDF1) and ABORTED merase3a (TOP3a) and RecQ-mediated instability 1 MICROSPORES (AMS), the latter of which encodes a (RMI1), which are components of the RTR (RecQ/Top3/ master regulator of tapetal development involved in the Rmi1) complex, are crucial for meiosis; mutations to the synthesis of lipidic and phenolic components essential corresponding Arabidopsis genes result in meiotic for pollen wall patterning and ﬂavonoid production (Gu defects and sterility. Analyses of tomato plants indicated et al. 2014; Sorensen et al. 2003; Zhu et al. 2008). In the the mutation in the top3a mutant is lethal to embryos, ms10 mutant, the expression levels of Soly- whereas the mutation in the rmi1 mutant does not c03g113530, Solyc08g062780, and Solyc04g008420, cause abnormalities in somatic DNA repair or meiosis which are homologs of AtTDF1, AtAMS, and MALE (Xing et al. 2012). Meiotic crossovers generate genetic STERILITY1 (AtMS1), respectively, are downregulated. diversity but improper crossover frequency can disrupt In addition to ms10 , the tomato male sterility 32 meiosis and cause pollen sterile in many plant species. A (ms32) mutant fails to undergo meiosis; its mutated group of genes that exert the function for limiting locus was mapped to a putative gene (Solyc01g081100) meiotic recombination have been identiﬁed in Ara- homologous to the Arabidopsis bHLH89/91 gene (Liu bidopsis, including Fanconi anemia of complementation et al. 2019). Moreover, the Solyc01g081100 expression group M (FANCM), Recombinant Escherichia coli ATP- level is downregulated in ms10 , suggesting that dependent DNA helicase (RECQ) and AAAATPase FIDGE- bHLH89/91 function downstream of DYT1 in tomato. In TIN-LIKE-1 (FIGL1). In contrast to the fact that loss of Arabidopsis, AMS has been reported to interact with function of these genes individually increases the bHLH89/91 to regulate the expression of MYB80, which crossover frequency and has little effect on fertility in promotes the sporopollenin synthesis for pollen wall Arabidopsis (Mieulet et al. 2018), the rice Osﬁgl1 mutant formation (Ferguson et al. 2017; Lou et al. 2014; Wang gives rise to aborted pollen, which may result from et al. 2018; Xiong et al. 2016; Zhang et al. 2007). The abnormal chromosome behavior during meiosis (Zhang rice bHLH protein UNDEVELOPED TAPETUM (OsUDT1), et al. 2017). Similarly, the tomato Slﬁgl1 mutant is also a putative homolog of AtDYT1, acts after initiation of the completely sterile, supporting the essential role of tapetum in an analogous manner to AtDYT1 (Jung et al. SlFIGL1 for fertility (Mieulet et al. 2018). To date, a few 2005). Moreover, a couple of important genes that are studies have been conducted on meiosis in tomato, essential for tapetum development have been cloned which has resulted in the identiﬁcation and characteri- from male-sterile rice mutants, including TAPETUM zation of several genes involved in meiosis. For example, DEGENERATION RETADATION (TDR) and OsMYB80, silencing MUTS-HOMOLOG 2 (MSH2), which encodes a which are homologs of AtAMS and AtMYB80, respec- protein that recognizes and repairs errors in DNA tively (Han et al. 2021; Pan et al. 2020; Phan et al. 2011; sequences, disrupts tomato male meiosis where half of Wilson and Zhang 2009). The functional similarity the meiocytes stalled at the zygotene stage or combined shared among these genes in both dicots and monocots to form diploid tetrads, which substantially inhibits suggest that the DYT1-TDF1-AMS-MYB80 transcrip- normal pollen formation (Sarma et al. 2018; Wang et al. tional cascade might also play an essential and 2021). The Author(s) 2023 aBIOTECH The post-meiosis pollen developmental stage is pathways are involved in pollen mitosis in tomato. microgametogenesis, in which microspores form pollen Recent research demonstrated that SlSWEET5b facili- grains via cellular mitosis. This process depends on the tates tomato pollen mitosis and maturation by mediat- asymmetrical division of the microspore during pollen ing the transport of apoplasmic hexose into developing mitosis I (PMI), which is essential for establishing male pollen cells (Ko et al. 2022), while SlMAPK20 is neces- germ cells (McCormick 2004). During mitosis in somatic sary for the uninucleate-to-binucleate transition of cell, the division site is marked by a circumferential tomato pollen cells, because it regulates anther sugar band of microtubules, called the preprophase band. metabolism (Chen et al. 2018). The molecular and reg- Although no obvious preprophase bands are observed ulatory mechanisms underlying the effects of sugar-re- in microspores before division, the migration of micro- lated signaling pathways on pollen mitosis will need to spore nuclear is sensitive to colchicine, suggesting the be more precisely characterized in future studies. involvement of a microtubule system (Twell et al. 1998). Thus, the ﬁne mapping of male sterility-related genes Compelling evidence comes from studies of the orchid and the identiﬁcation of genes associated with genic Phalaenopsis, in which a specialized generative pole male sterility in tomato have deepened our under- microtubule system appears at the future generative cell standing of the molecular basis of male reproductive pole prior to nuclear migration (Brown and Lemmon development and may increase the utility of biotech- 1991). In Arabidopsis, mutations in microtubule-related nology-based male sterility systems in hybrid breeding genes impact asymmetrical division of microspores and programs. cause abnormal male germline formation, ultimately lead to male sterility, such as gemini pollen1 (gem1), two-in-one (tio) and kinesin- 12A/ 12B (Liu and Qu ADAPTIVE RESPONSES OF TOMATO MALE 2008; Twell 2011). Given that the microtubule system REPRODUCTIVE DEVELOPMENT TO ABIOTIC plays an important role in directing and maintaining STRESSES nuclear migration, one can expect that it might act in response to cellular signals or polarity determinants Extreme environmental stresses, including excessive within the cytoplasm. However, the underlying mecha- heat, cold, and drought, adversely affect male fertility in nisms are still unclear so far. Mutations to cell-cycle ﬂowering plants and cause substantial crop yield losses. regulators in Arabidopsis can impair the progression of For example, high-temperature stress can negatively pollen mitosis with lethal consequences for gameto- affect male reproductive structures and processes (e.g., phytes (Liu and Qu 2008; Liu et al. 2008; Takatsuka stigma exsertion or anther indehiscence), leading to et al. 2015). Loss-of-function of genes related to decreased pollen dispersal and fruit set in tomato (Pan microtubules or cell-cycle regulators in tomato also et al. 2019; Sato et al. 2002). In most plants, the pro- directly affects the asymmetrical division of pollen cells cesses from meiosis to PMI are especially vulnerable to (Yang et al. 2022). In addition, some intracellular abiotic stress. When pollen development reaches the metabolites help regulate pollen mitosis. For example, in meiotic stage, the tapetal cells are highly metabolically Arabidopsis, the auxin ﬂow in anthers affects pollen active, with 20- to 40-fold increases in mitochondrial development by regulating PMI (Feng et al. 2006). activities (Parish et al. 2012). There is increasing evi- Additionally, the mutations in the yuc2yuc6 double dence of the link between abiotic stress-induced male mutant result in arrested PMI and a lack of viable pollen sterility and tapetal dysfunction (Go´mez et al. 2015). (Yao et al. 2018). Thus, auxin is vital for asymmetrical Excessive heat is not the only temperature-related pollen cell division. In tomato, a mutation to SlPIF3 stress that can decrease crop yields. Even mild tem- prevents the production of viable pollen grains because perature ﬂuctuations have induced grain yield losses of of the associated arrested PMI. Compared with wild- approximately 10%, 5.5%, and 3.8% per 1 C increase type tomato plants, the Slpif3 mutant has a substantially in rice, wheat, and maize, respectively (Lobell et al. lower anther auxin content and abnormal microtubule- 2011; Peng et al. 2004; Tashiro and Wardlaw 1989). An and cell-cycle-related gene expression levels (Yang et al. exposure to heat stress can induce male sterility in 2022). The application of exogenous auxin downregu- Arabidopsis, rice, wheat, and tomato by impairing lates the expression of cyclin kinase inhibitor genes tapetum differentiation and microsporogenesis, acti- (SlKRP2 and SlKRP4), while also partially rescuing the vating tapetal PCD prematurely, and inhibiting the pollen viability of the Slpif3 mutant, suggesting that dehiscence of anthers (Parish et al. 2012). At the auxin regulates tomato PMI by modulating the expres- molecular level, heat stress induces oxidative damage, sion of genes related to microtubules and the cell cycle. prevents proteins from folding correctly, and disturbs Furthermore, sugar metabolism-associated signaling hormone homeostasis (Fig. 2A). In response to heat The Author(s) 2023 aBIOTECH Fig. 2 Regulatory pathway of the tomato anther and pollen development in response to abiotic stress. A High-temperature (HT) stress induces ROS production and the tomato tapetal PCD process, leading to male sterility. An exposure to HT stress also increases the HSF and UPR expression levels, thereby enhancing the ability of tomato anthers and pollen grains to tolerate heat stress. B Low-temperature (LT) stress leads to abnormal anther m A levels and increased ABA contents in tomato, which adversely affects sugar metabolism by decreasing CWIN expression levels and delaying tapetal PCD degradation, ultimately resulting in male sterility. Moreover, LT stress enhances the production of SlPIF4, which interacts with SlDYT1 and induces SlTDF1 expression, which leads to delayed tapetal PCD. Drought inhibits tapetal degradation through the ABA and IAA signaling pathways. Upward and downward pointing red arrows indicate signiﬁcant increases and decreases, respectively. The dashed line indicates a putative role or relationship stress, mitochondria increase the production of reactive that produce antioxidant enzymes that eliminate oxygen species (ROS) via enhanced aerobic metabolism excessive ROS in cells (Parish et al. 2012). Increases in and cause oxidative damage and cell death, with crucial ROS levels reportedly induce the production of detoxi- effects on tapetal PCD in Arabidopsis, rice, and tomato ﬁcation-related enzymes in wheat pollen (Kumar et al. (Parish et al. 2012; Zhang et al. 2021). A recent study 2014). Additionally, increasing ROS contents can showed that loss-of-function mutations to DWARF upregulate the expression of HEAT SHOCK TRANSCRIP- (DWF) and BRASSINAZOLE-RESISTANT1 (BZR1) alter the TION FACTOR A1 (HsfA1), which substantially activates timing of ROS production and delay tapetal PCD in the expression of heat responsive genes. In Arabidopsis tomato (Yan et al. 2020). These ﬁndings provide evi- and tomato hsfa1 mutants, the expression levels of dence that ROS homeostasis in anthers contributes to many HS-responsive genes are lower than normal, the regulation of tapetal cell degeneration. Heat stress resulting in vegetative tissues with HS-insensitive phe- promotes the production of protein disulﬁde isomerase notypes (Mishra et al. 2002; Yoshida et al. 2011). Many 9 (PDI9), which affects nascent and misfolded proteins HSF and HSP genes are highly expressed in tomato in the endoplasmic reticulum; a mutation to the corre- microsporocytes and microspores, and their expression sponding gene decreases pollen viability at high tem- levels may be further increased by heat stress (Cha- peratures (Feldeverd et al. 2020). Plants rely on diverse turvedi et al. 2013). For example, SlHsfA2 regulates the mechanisms to withstand heat stress, including the expression of several HS-responsive genes and main- production of antioxidants and ROS scavengers as well tains pollen viability in plants exposed to heat stress as the induction of heat shock transcription factors during meiosis in the microspore stage, suggestive of (HSFs) and heat shock proteins (HSPs) (Chaturvedi et al. the importance of HsfA2 for pollen thermotolerance 2013). Heat stress may also activate a regulatory loop in (Fragkostefanakis et al. 2016). The contribution of which accumulating ROS modulate signaling cascades AtHsfA5 to pollen thermotolerance was revealed in an The Author(s) 2023 aBIOTECH earlier study in which the pollen abortion rate was negative correlation between the anther ABA content relatively high for the Athsfa5 mutant because of and pollen fertility (Oliver et al. 2007). In tomato, an defective HS responses (Renˇ a´k et al. 2014). Phytohor- exposure to cold stress signiﬁcantly increases anther mone signaling pathways typically mediate plant ABA levels, but the expression of SlCWIN7, which is responses to abiotic stress. Excessive heat causes the homologous to the rice gene OsINV4, signiﬁcantly abscisic acid (ABA) level to increase in rice anthers, decreases, suggesting that low temperatures disrupt whereas the IAA and GA contents decrease, leading to a anther sugar metabolism, which leads to pollen sterility decrease in pollen fertility (Zhang et al. 2021). The (Yang et al. 2021). Reversible epigenetic modiﬁcations application of exogenous auxin can reverse the male typically occur in developing plants in response to sterility of barley plants exposed to high temperatures, environmental stress. At low temperatures, N6-methy- demonstrating that auxin defection was an essential ladenosine (m A) levels decrease in tomato anthers, factor responsible for the heat stress-induced male which results in the altered transcription of many pollen sterility (Sakata et al. 2010). Notably, the AUXIN development-related genes (Yang et al. 2021). These RESPONSE FACTOR17 (ARF17) was reported to directly ﬁndings suggest m A may inﬂuence tomato pollen regulate the expression of CALLOSE SYNTHASE5 (CalS5), development under cold conditions. Similar to cold the key gene for callose biosynthesis. The miR160 reg- stress, drought conditions can interfere with tapetal ulated expression of ARF17 is also required for its development by preventing or delaying the induction of function during anthers development in Arabidopsis PCD in developing tomato pollen grains (Lamin-Samu (Wang et al. 2017; Yang et al. 2013). Both ABA and GA et al. 2021). Analyses of transcription levels and hor- are candidate signaling molecules that affect tapetal mone metabolism showed that in tomato anthers, development by regulating carbohydrate availability in drought stress upregulates the expression of genes the tapetum and microspores under abiotic stresses related to tapetum development and ABA homeostasis, (Zhang et al. 2021). whereas it has the opposite effect on the expression of Cold stress is another prevalent abiotic factor affect- sugar metabolism-associated genes, leading to ing the growth and development of plants, especially increased ABA levels and decreased soluble sugar con- subtropical vegetable crops. In Arabidopsis and rice, tents, which is consistent with what has been reported cold stress usually delays or inhibits tapetum regener- for other crops (Ji et al. 2011; Oliver et al. 2007). These ation by disrupting tapetal PCD, resulting in infertile results imply that in tomato, drought stress has detri- pollen (Zhang et al. 2021). In developing tomato anthers mental effects on the metabolism of carbohydrates and and pollen grains, PCD-triggered tapetum degradation is hormones. The molecular mechanisms linking tapetal initiated during the tetrad stage, intensiﬁes from the development and anther sugar and ABA homeostasis early-to-late uninucleate stage, and is undetectable at remain unclear. Future research will need to elucidate the binucleate pollen stage. Cold stress in tomato leads the cold- and/or drought-induced changes to these to irregular hypertrophy and tapetum vacuolation mechanisms that lead to tapetal dysfunction. because of delayed PCD, which subsequently leads to pollen abortion (Fig. 2B) (Pan et al. 2021; Yang et al. 2021). In contrast, pollen grains develop normally in the CONCLUSIONS AND FUTURE PERSPECTIVES tomato Slpif4 mutant under cold stress conditions because the inhibited activation of SlTDF1 makes the Increases in the global population as well as climate tapetum relatively insensitive to low temperatures changes are major issues that must be addressed to (Fig. 2B) (Pan et al. 2021). The inhibition of invertase maintain agricultural production and food security. In may be associated with tapetal hypertrophy and vac- addition to increasing crop yields, minimizing abiotic uolation. For example, during male gametogenesis in stress-induced production losses is a major objective rice, low-temperature stress causes ABA to accumulate, among plant researchers. Thoroughly characterizing the which may suppress the expression of the tapetum- mechanism regulating male fertility and identifying speciﬁc cell wall invertase gene OsINV4 and the novel stress resistance genes associated with male monosaccharide transporter genes OsMST8 and reproductive development may enable the generation of OsMST7, leading to abnormalities in anther sugar stress-resistant germplasm resources suitable for metabolism and male sterility (Oliver et al. 2005). biotechnology-based crop breeding. Research regarding Abscisic acid has vital functions related to plant devel- reproductive stress tolerance has continued to progress opment and mediates responses to abiotic stress. because multiple strategies have been applied. For Increased ABA levels improve plant abiotic stress tol- example, protein phase separations have been revealed erance during the vegetative growth stage, but there is a to contribute to plant adaptive responses to cellular pH The Author(s) 2023 aBIOTECH Science Foundation of China (U1903202) and Major Research Plan changes, temperature ﬂuctuations, and oxidative stress. of National Natural Science Foundation of China (31991183) to In Arabidopsis, a prion-like domain in ELF3 functions as C.X. and China National Postdoctoral Program for Innovative a putative thermo-sensor to undergo protein phase Talents (BX20220336) to D.Y. transition that results in the formation of liquid droplets in response to increasing temperatures (Jung et al. Data availability Data sharing not applicable to this article as no datasets were generated or analysed during the current study. 2020). The oxidation in the tomato shoot apical meris- tem triggers protein phase separations that enable TMF Declarations to bind to the promoter of the ﬂoral identity gene ANANTHA to repress its expression (Huang et al. 2021). Conﬂict of interest The authors declare that they have no com- peting interests. The reversible protein phase separation promoted by changing internal and external conditions is responsible Open Access This article is licensed under a Creative Commons for the ﬂexibility with which plants respond to global Attribution 4.0 International License, which permits use, sharing, climate changes; this may represent a new abiotic stress adaptation, distribution and reproduction in any medium or for- mat, as long as you give appropriate credit to the original mechanism inﬂuenced by plant developmental cues, author(s) and the source, provide a link to the Creative Commons especially those related to reproductive development. licence, and indicate if changes were made. The images or other Stress resistance is typically a complex and polygenic third party material in this article are included in the article’s trait. Developing novel plant lines with desirable traits Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s through polygenic editing is a considerable challenge. Creative Commons licence and your intended use is not permitted There are numerous extant wild relatives of tomato that by statutory regulation or exceeds the permitted use, you will are highly tolerant to various stresses. Therefore, the de need to obtain permission directly from the copyright holder. To novo domestication of wild tomato species has been view a copy of this licence, visit http://creativecommons.org/ proposed as a viable alternative for creating climate- licenses/by/4.0/. smart crops via genome engineering (Li et al. 2018a). 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Journal

aBIOTECH – Springer Journals

Published: Mar 1, 2023

Keywords: Tomato; Climate change; Male; Reproductive development

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Relationships between tapetum, loculus, and pollen during development

Pacini, E
Tomato stigma exsertion induced by high temperature is associated with the jasmonate signalling pathway

Pan, C; Yang, D; Zhao, X; Jiao, C; Yan, Y; Lamin-Samu, AT; Wang, Q; Xu, X; Fei, Z; Lu, G
osmyb80 regulates anther development and pollen fertility by targeting multiple biological pathways

Pan, X; Yan, W; Chang, Z; Xu, Y; Luo, M; Xu, C; Chen, Z; Wu, J; Tang, X
PIF4 negatively modulates cold tolerance in tomato anthers via temperature-dependent regulation of tapetal cell death

Pan, C; Yang, D; Zhao, X; Liu, Y; Li, M; Ye, L; Ali, M; Yu, F; Lamin-Samu, AT; Fei, Z
Tapetal development and abiotic stress: a centre of vulnerability

Parish, RW; Phan, HA; Iacuone, S; Li, SF
Rate of meristem maturation determines inflorescence architecture in tomato

Park, SJ; Jiang, K; Schatz, MC; Lippman, ZB
Rice yields decline with higher night temperature from global warming

Peng, S; Huang, J; Sheehy, JE; Laza, RC; Visperas, RM; Zhong, X; Centeno, GS; Khush, GS; Cassman, KG
The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana

Phan, HA; Iacuone, S; Li, SF; Parish, RW
A new link between stress response and nucleolar function during pollen development in Arabidopsis mediated by AtREN1 protein

Reňák, D; Gibalová, A; Šolcová, K; Honys, D
The parthenocarpic hydra mutant reveals a new function for a SPOROCYTELESS-like gene in the control of fruit set in tomato

Rojas-Gracia, P; Roque, E; Medina, M; Rochina, M; Hamza, R; Angarita-Díaz, MP; Moreno, V; Pérez-Martín, F; Lozano, R; Cañas, L
Auxins reverse plant male sterility caused by high temperatures

Sakata, T; Oshino, T; Miura, S; Tomabechi, M; Tsunaga, Y; Higashitani, N; Miyazawa, Y; Takahashi, H; Watanabe, M; Higashitani, A
Pollen development at high temperature and role of carbon and nitrogen metabolites

Santiago, JP; Sharkey, TD
MutS-Homolog2 silencing generates tetraploid meiocytes in tomato (Solanum lycopersicum)

Sarma, S; Pandey, AK; Sharma, K; Ravi, M; Sreelakshmi, Y; Sharma, R
Determining critical pre- and post-anthesis periods and physiological processes in Lycopersicon esculentum Mill. exposed to moderately elevated temperatures

Sato, S; Peet, MM; Thomas, JF
Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana

Schiefthaler, U; Balasubramanian, S; Sieber, P; Chevalier, D; Wisman, E; Schneitz, K
Effects of jasmonate on ethylene function during the development of tomato stamens

Schubert, R; Grunewald, S; Von, SL; Hause, B
Genetic and biochemical mechanisms of pollen wall development

Shi, J; Cui, M; Yang, L; Kim, YJ; Zhang, D
A cellular mechanism underlying the restoration of thermo/photoperiod-sensitive genic male sterility

Shi, QS; Lou, Y; Shen, SY; Wang, SH; Zhou, L; Wang, JJ; Liu, XL; Xiong, SX; Han, Y; Zhou, HS
The Arabidopsis aborted microspores (ams) gene encodes a MYC class transcription factor

Sorensen, AM; Kröber, S; Unte, US; Huijser, P; Dekker, K; Saedler, H
Cyclin-dependent kinase-activating kinases CDKD;1 and CDKD;3 are essential for preserving mitotic activity in Arabidopsis thaliana

Takatsuka, H; Umeda-Hara, C; Umeda, M
A comparison of the effect of high temperature on grain development in wheat and rice

Tashiro, T; Wardlaw, IF
Male gametogenesis and germline specification in flowering plants

Twell, D
Asymmetric division and cell-fate determination in developing pollen

Twell, D; Park, SK; Lalanne, E
Fine regulation of ARF17 for anther development and pollen formation

Wang, B; Xue, JS; Yu, YH; Liu, SQ; Zhang, JX; Yao, XZ; Liu, ZX; Xu, XF; Yang, ZN
The regulation of sporopollenin biosynthesis genes for rapid pollen wall formation

Wang, K; Guo, ZL; Zhou, WT; Zhang, C; Zhang, ZY; Lou, Y; Xiong, SX; Yao, XZ; Fan, JJ; Zhu, J
Meiosis in crops: from genes to genomes

Wang, Y; Van Rengs, WMJ; Zaidan, MWAM; Underwood, CJ
The molecular mechanism of sporocyteless/nozzle in controlling Arabidopsis ovule development

Wei, B; Zhang, J; Pang, C; Yu, H; Guo, D; Jiang, H; Ding, M; Chen, Z; Tao, Q; Gu, H
From Arabidopsis to rice: pathways in pollen development

Wilson, ZA; Zhang, DB
A two-in-one breeding strategy boosts rapid utilization of wild species and elite cultivars

Xie, Y; Zhang, T; Huang, X; Xu, C
Functional identification of a novel F-box/FBA gene in tomato

Xing, L; Li, Z; Khalil, R; Ren, Z; Yang, Y
The transcription factors MS188 and AMS form a complex to activate the expression of CYP703A2 for sporopollenin biosynthesis in Arabidopsis thaliana

Xiong, SX; Lu, JY; Lou, Y; Teng, XD; Gu, JN; Zhang, C; Shi, QS; Yang, ZN; Zhu, J
Brassinosteroid-mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato

Yan, MY; Xie, DL; Cao, JJ; Xia, XJ; Shi, K; Zhou, YH; Zhou, J; Foyer, CH; Yu, JQ
The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein

Yang, WC; Ye, D; Xu, J; Sundaresan, V
AUXIN RESPONSE FACTOR17 is essential for pollen wall pattern formation in Arabidopsis

Yang, J; Tian, L; Sun, MX; Huang, XY; Zhu, J; Guan, YF; Jia, QS; Yang, ZN
RNA N6-Methyladenosine responds to low-temperature stress in tomato anthers

Yang, D; Xu, H; Liu, Y; Li, M; Ali, M; Xu, X; Lu, G
Phytochrome interacting factor 3 regulates pollen mitotic division through auxin signalling and sugar metabolism pathways in tomato

Yang, D; Liu, Y; Ali, M; Ye, L; Pan, C; Li, M; Zhao, X; Yu, F; Zhao, X; Lu, G
Auxin production in diploid microsporocytes is necessary and sufficient for early stages of pollen development

Yao, X; Tian, L; Yang, J; Zhao, YN; Zhu, YX; Dai, X; Zhao, Y; Yang, ZN
The contributions of sporophytic tapetum to pollen formation

Yao, X; Hu, W; Yang, Z
Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression

Yoshida, T; Ohama, N; Nakajima, J; Kidokoro, S; Mizoi, J; Nakashima, K; Maruyama, K; Kim, JM; Seki, M; Todaka, D
Regulation of Arabidopsis tapetum development and function by Dysfunctional Tapetum1 (DYT1) encoding a putative bHLH transcription factor

Zhang, W; Sun, Y; Timofejeva, L; Chen, C; Grossniklaus, U; Ma, H
Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis

Zhang, ZB; Zhu, J; Gao, JF; Wang, C; Li, H; Li, H; Zhang, HQ; Zhang, S; Wang, DM; Wang, QX
The Rice AAA-ATPase OsFIGNL1 Is essential for male meiosis

Zhang, P; Zhang, Y; Sun, L; Sinumporn, S; Yang, Z; Sun, B; Xuan, D; Li, Z; Yu, P; Wu, W
Understanding the molecular mechanism of anther development under abiotic stresses

Zhang, Z; Hu, M; Xu, W; Wang, Y; Huang, K; Zhang, C; Wen, J
Defective in Tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis

Zhu, J; Chen, H; Li, H; Gao, JF; Jiang, H; Wang, C; Guan, YF; Yang, ZN
Slowing development restores the fertility of thermo-sensitive male-sterile plant lines

Zhu, J; Lou, Y; Shi, QS; Zhang, S; Zhou, WT; Yang, J; Zhang, C; Yao, XZ; Xu, T; Liu, JL

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Molecular regulation of tomato male reproductive development

Molecular regulation of tomato male reproductive development

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Molecular regulation of tomato male reproductive development

Molecular regulation of tomato male reproductive development

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