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aBIOTECH https://doi.org/10.1007/s42994-022-00089-y aBIOTECH REVIEW Genetic architecture and molecular regulation of sorghum domestication 1,2 1& 1& 1,2& Fengyong Ge , Peng Xie , Yaorong Wu , Qi Xie State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China Received: 28 September 2022 / Accepted: 28 November 2022 Abstract Over time, wild crops have been domesticated by humans, and the knowledge gained from parallel selection and convergent domestication-related studies in cereals has contributed to current techniques used in molecular plant breeding. Sorghum (Sorghum bicolor (L.) Moench) is the world’s ﬁfth-most popular cereal crop and was one of the ﬁrst crops cultivated by ancient farmers. In recent years, genetic and genomic studies have provided a better understanding of sorghum domestication and improve- ments. Here, we discuss the origin, diversiﬁcation, and domestication processes of sorghum based on archeological discoveries and genomic analyses. This review also comprehensively summarized the genetic basis of key genes related to sorghum domestication and outlined their molecular mechanisms. It highlights that the absence of a domestication bottleneck in sorghum is the result of both evolution and human selection. Additionally, understanding beneﬁcial alleles and their molecular interactions will allow us to quickly design new varieties by further de novo domestication. Keywords Domestication, Genetic basis, Molecular mechanism, Genes, Sorghum INTRODUCTION geographical regions and adapt to the local environ- ment, resulting in a diversiﬁcation of domesticated Crop domestication has contributed to the rise of agri- alleles and the formation of landraces; in stage 4, culture and the transition away from hunting and humans deliberately breed improved cultivars to meet gathering, laying the groundwork for modern human the demands of modern diets (Gaut et al. 2018; Lenser civilization (Purugganan and Fuller 2009). Evidence and Theissen 2013). Compared with their wild ances- collected from archeological discoveries and genetic and tors, domesticated crops share some common morpho- genomic studies indicates that crop domestication is a logical and physiological characteristics, which is known protracted process rather than a short, discrete event as domestication syndrome, including loss of seed (Purugganan 2019). In general, the domestication pro- shattering (non-shattering), loss of seed dormancy, seed cess can be divided into four stages: in stage 1, humans enlargement, synchronous germination, and changes in harvest and consume wild plants; in stage 2, humans tiller number and stature (Gepts 2014; Stetter et al. deliberately cultivate crops, resulting in genetic bottle- 2017). These traits typically occur under parallel/con- necks and a decline in wild alleles (Doebley et al. 2006); vergent domestication among different crops (Lenser in stage 3, domesticated plants expand to new and Theissen 2013; Purugganan 2019). The plant domestication center refers to the original geographic region where a speciﬁc species was domesticated. Three & Correspondence: email@example.com (P. Xie), yrwu@genet- main cereal crops (rice, wheat, and maize) supply more ics.ac.cn (Y. Wu), firstname.lastname@example.org (Q. Xie) The Author(s) 2022 aBIOTECH than 50% of human calories, out of * 5500 food crops from archeological discoveries (Ananda et al. 2020). cultivated worldwide (Ross-Ibarra et al. 2007; Zhao Some studies have reported the potential evolutionary et al. 2021), and were originally domesticated in East history and dispersal route of domesticated sorghum Asia, the Middle East, and Central America, respectively (Burgarella et al. 2021; Fuller and Stevens 2018; Ven- (Gepts 2014; Larson et al. 2014). kateswaran et al. 2019; Winchell et al. 2018). It has Sorghum (Sorghum bicolor (L.) Moench) is the ﬁfth- been proposed that sorghum was ﬁrst domesticated in most popular cereal crop in the world and is a staple the eastern Sahelian zone in approximately 4000 BC and food for more than 500 million people in Africa and Asia propagated to South Asia approximately 1000 years (Xin et al. 2021; FAOSTAT, https://www.fao.org/faostat/ later (Winchell et al. 2017, 2018). Then, sorghum was en/#data). It is estimated that sorghum was ﬁrst culti- introduced to China and domesticated into Chinese vated as a food source in the Sahelian belt of Africa and kaoliang (Zhang and Ping 2022). was originally domesticated in central eastern Sudan The genus Sorghum consists of 23 or 24 species, approximately 6000 to 4000 years ago (Winchell et al. though the taxonomy of this genus is still being debated 2017). In addition to being a valuable source of calories, (Ananda et al. 2020; Ohadi et al. 2018). Sorghum bicolor sorghum can also be used as ﬁber, forage, and fuel (Hao (L.) Moench subsp. bicolor contains all cultivated sor- et al. 2021; Silva et al. 2021; Xie and Xu 2019). Since ghum varieties, which were derived from the wild pro- sorghum was domesticated and evolved in arid and genitor S. bicolor subsp. verticilliﬂorum (formerly semiarid ecosystems, it exhibits strong resistance to known as subsp. arundinaceum), which is widely dis- many abiotic stresses, such as drought, high light, bar- tributed in Africa (Berenji et al. 2011; Wet and Harlan renness, salt, and alkalinity, making it an ideal resistant 1971; Wet and Huckabay 1967). Instead of the complex plant resource to meet the modern demands of crop early classiﬁcation that divided cultivated sorghum into breeding to ensure food security under climate change 158 varieties, Harlan and de Wet proposed a revised (Ma et al. 2020; Prasad et al. 2021; Varoquaux et al. version that has been accepted by the following 2019; Xie and Xu 2019; Yang et al. 2020). Apart from the researchers (Harlan and de Wet 1972). According to the archeological and fossil discoveries, recent evidence simpliﬁed morphological characteristics of the spikelet from genetic and genomic studies of sorghum provides and head type, cultivated sorghum can be classiﬁed into clues about its domestication at the molecular level ﬁve basic races: bicolor, guinea, caudatum, kaﬁr, and (Baye et al. 2022; Wu et al. 2022, 2019; Xie et al. 2022; durra. Race bicolor is considered the oldest race, and its Zhang et al. 2018; Zhou et al. 2021). With the help of seeds are more tightly covered by glumes than those of modern advanced biotechnologies, such as synthetic the other four races (de Wet and Shechter 1977). Race biology and gene editing techniques, we can rapidly guinea likely evolved in West Africa and adapted to improve current cultivars or create new crops by de humid habitats with a loose head type and glumes novo domestication (such as in tomato and rice) to opening at a large angle (de Wet et al. 1972). Race durra address the crises caused by food deﬁciency once we could be derived from hybridization between the race understand the underlying genetic basis of domestica- bicolor and local wild species in India (Harlan and tion-related genes (Li et al. 2018;Yuetal. 2021). Stemler 1976). It has a compact panicle and lower In this review, we discuss widely accepted opinions glumes than bicolor. Glumes typically have different about sorghum domestication and characteristics based textures between the tip and the base (de Wet and on archeological records and genomic studies. We Shechter 1977). Race kaﬁr shows glumes varying in comprehensively and systematically summarized the length, derived from early bicolor or independently genetic basis and molecular mechanisms of major sor- evolved from the local wild race in South Africa. The ghum domestication-related genes. The conclusions origin of race caudatum has not been fully determined. regarding the artiﬁcial selection of sorghum will accel- It could be directly selected from early bicolor with erate sorghum breeding processes when combined with lower glumes and has become a major sorghum donor advanced biotechnologies. widely distributed in eastern Nigeria, Sudan, and Uganda (Shechter and de Wet 1975). The proposed original domestication center, main distribution, and SORGHUM ORIGIN, DISTRIBUTION, spikelet morphology of ﬁve cultivated sorghum races in AND CLASSIFICATION Africa are depicted in Fig. 1. During agricultural cultivation, sorghum can be Although some issues are still under debate, it is widely classiﬁed into different subgroups based on its end use. accepted that sorghum originated from Africa in In the literature, domesticated sorghum has been clas- approximately 7500 BC, based on evidence gathered siﬁed into grain sorghum, sweet sorghum, forage The Author(s) 2022 aBIOTECH subsequently improved genome assembly version annotated 34,211 genes (McCormick et al. 2018). Additionally, the reference genomes of the sorghum cultivar Tx430 and a sweet sorghum line Rio were also released in recent years (Cooper et al. 2019; Deschamps et al. 2018). The genome sequences of the other three sorghum accessions, BTx642, RTx430, and SC187, are also available on the Phytozome website (https://phy tozome-next.jgi.doe.gov/). A comparison of genomic and transcriptomic data between BTx623 and Rio revealed structural variations and differentially expressed genes involved in sugar metabolism (Cooper et al. 2019). The pangenome of cultivated and wild sorghum revealed new annotated genes and presence and absence varia- tions (PAVs) that could play an important role in sor- Fig. 1 Domestication centers, original distribution, and spikelet morphology of ﬁve domesticated sorghum races (bicolor, guinea, ghum domestication and diversiﬁcation (Ruperao et al. caudatum, kaﬁr, and durra). The early bicolor race was distributed 2021; Tao et al. 2021). in the eastern Sahelian zone and spread to other African regions. Advancements in sequencing technology and bioin- Its seeds are more tightly covered than those of the other four formatics make it possible to analyze genetic informa- races. Race guinea probably evolved in West Africa and adapted to tion at the population level, increasing our knowledge of humid habitats with glumes opening at a large angle. Race kaﬁr is widely grown in South Africa, with glumes varying in length. Race the evolutionary trajectory on many species, such as caudatum is dominant in eastern Nigeria, Sudan, and Uganda, with rice, soybean, tomato, lettuce, and apricots (Groppi et al. a relatively lower glume coverage. Race durra could be derived 2021; Lin et al. 2014; Lu et al. 2020; Qin et al. 2021;Wei from the hybridization between race bicolor and the local wild et al. 2021). In sorghum, resequencing analysis of nine species in India, and then subsequently re-introduced to Africa. Arrows indicate the possible spreading routes of race durra. The archeological accessions discovered at Qasr Ibrim from gray background represents the Sahelian zone approximately 800 BC, as well as wild and cultivated sorghum genomes, revealed that there was no obvious sorghum, and biomass sorghum (Silva et al. 2021). domestication bottleneck in sorghum, but that there However, the boundary between forage and biomass was a gradual decline in genetic diversity. It also sorghum is unclear, and another classiﬁcation added induced an increase in deleterious mutations in culti- broom sorghum instead of biomass sorghum (Li and Yu vated sorghum lines, known as the ‘‘cost of domestica- 2022). Grain sorghum typically has larger seeds and a tion’’ (Gaut et al. 2018; Smith et al. 2019). Evidence from short lifespan, while sweet sorghum accumulates the genome information demonstrated the presence of abundant soluble sugars in its stem. Forage sorghum is occasional hybridization between the Asian durra type bred to feed animals with higher biomass and better and African bicolor type, which led to genetic rescue palatability. Broom sorghum with long panicles is used and diversiﬁcation in sorghum domestication. to produce traditional homemade brooms (Berenji et al. Hybridization or genetic introgression was also discov- 2011). The various morphological characteristics of ered between cultivated sorghum and their weedy or sorghum are due to evolution and artiﬁcial selection, wild relatives, indicating the occurrence of high-fre- indicating that there are abundant genetic resources quency active gene ﬂow in sorghum. This differs from related to these traits. other strict self-pollination crops (Ohadi et al. 2018). A recent population genetic study deepened our understanding of sorghum domestication and diversiﬁ- GENOMIC FOOTPRINTS OF SORGHUM cation at the whole-genome level. A total of 445 sor- DOMESTICATION ghum accessions were classiﬁed into seven subpopulations, including wild, sudangrass, landrace Morphological variation during crop evolution is mainly broom (LB), landrace grain (LG), improved grain (IG), determined by genetic modiﬁcation in the nucleotide improved sweet (IS), and ambiguous lines (AL), based sequence of the genome. Sorghum is a diploid crop on distinct phenotypic differentiation. Analysis of (2n =2x = 20). The whole-genome assembly of the whole-genome resequencing data also revealed the sorghum cultivar BTx623 was ﬁrst achieved using de existence of frequent genetic exchanges between LG and novo sequencing in 2009, and the reference genome size the wild type. LB lines, mostly collected from Asia, is approximately 730 Mb (Paterson et al. 2009). A received gene ﬂow from the common ancestor with LG, The Author(s) 2022 aBIOTECH while IS received gene ﬂows from both LB and sudan- Plant height and tillers grass (Wu et al. 2022). In addition, genomic regions with selection signals were identiﬁed in different Plant height is one of the most prominent target char- groups, and eight models based on the haplotype acteristics in crop breeding. Dwarﬁsm in crops can increase lodging resistance and decrease grain yield changes of domesticated genes were proposed. Among them, two important models represented soft selection loss. In rice and wheat, semidwarf varieties with deﬁ- ciencies in gibberellin biosynthesis and signaling path- with multiple domestication origins and hard selection with only one domestication event. Deep whole-genome ways were bred by breeders and subsequently initiated the ‘‘green revolution’’ (Wang et al. 2021). However, resequencing and analysis of a sorghum association panel (SAP) containing 400 sorghum accessions iden- dwarﬁsm is not a universal breeding goal for sweet or tiﬁed 18 genomic regions with signiﬁcant F peaks. forage sorghum due to the demand for varieties with st These peaks varied in the ﬁve typical domesticated tall and robust statures and high biomass. Additionally, races, which reﬂects evolutionary differences and rela- decreased plant height is widely selected in grain sor- tionships during sorghum domestication. More impor- ghum or other races with high grain yield. tantly, these regions overlap with some previously It has been reported that sorghum plant height is controlled by four independent loci, named Dw1, Dw2, reported quantitative trait loci (QTLs), indicating that the potential genetic mechanism underlying domesti- Dw3, and Dw4 (Quinby and Martin 1954). Recessive mutations of each locus could lead to decreases in plant cation-related traits could be uncovered in the future (Boatwright et al. 2022). height. The underlying genes of the Dw1, Dw2, and Dw3 loci have been cloned. Dw3 encodes a protein containing transmembrane domains and ATP-binding domains. It GENETIC DISSECTION OF DOMESTICATION- functions in transporting auxin from the middle to RELATED TRAITS IN SORGHUM lower stem tissues in a light-dependent manner. A nonfunctional allele with an 882 bp duplication in the ﬁfth exon of Dw3 was found in the dw3 mutant. This Studies analyzing the genetics and molecular biology of sorghum have identiﬁed many genes related to sorghum mutation caused the dwarf phenotype with a reduction in internode length. However, the unequal crossing over domestication, and the underlying genetic basis has been well elucidated. In the following text, we summa- of this duplication led to an unstable dwarf phenotype as a few accidental offspring individuals with tall plant rize the major domesticated genes in sorghum and introduce their molecular mechanisms. These genes are height (Multani et al. 2003). Dw1 was ﬁnely mapped to a 33 kb region on chromosome 6, and mostly involved in panicle-related traits, such as seed shattering, tannin content, awn and glume coverage, Sobic.009G229800 was considered the candidate gene while others are related to stem juiciness, ﬂowering, (Hilley et al. 2016). Dw1 encodes a putative membrane and plant architecture, including plant height and tiller protein with a higher expression level in elongating number (Fig. 2 and Table 1). middle stems. The dwarf parent 80M carries the dw1 Fig. 2 Plant architecture of wild and weedy sorghum and domesticated sorghum cultivar. The major genes controlling sorghum domestication-related traits are SbTB1 (reduced tillers), Dw1, Dw2, and Dw3 (dwarﬁsm), Dry (stem juiciness), SbPRR37, Ma2, PhyB, Ma4, PhyC, and SbGhd7 (early-ﬂowering time in LD), GC1 (naked grains), awn1 (awnless), Sh1 and SpWRKY (non-shattering), and Tan1 and Tan2 (non-tannin). LD long day, Sb, Sorghum bicolor The Author(s) 2022 aBIOTECH Table 1 Genes that potentially underlie domestication, diversiﬁcation and improvement of sorghum Trait Gene Gene loci Gene category Causative change References name Plant Dw1 Sobic.009G229800 Uncharacterized SNP in second exon causing premature stop Yamaguchi et al. 2016 height Dw2 Sobic.006G067700 AGC protein kinase 2 bp deletion in ﬁrst exon causing frameshift Hilley et al. 2017; and truncated protein Oliver et al. 2021 Dw3 Sobic.007G163800 ABC transporter Duplication in ﬁfth exon Multani et al. 2003 Dw4 Unknown Unknown NA Quinby and Martin Tillers SbTB1 Sobic.001G121600 TCP domain SNP in promoter Kebrom et al. 2006; transcription Wu et al. 2022 factor Stem Dry or D Sobic.006G147400 NAC domain Large deletion Fujimoto et al. 2018; juiciness transcription Zhang et al. 2018 factor Flowering SbPRR37 Sobic.006G057866 PRR protein Sbprr37-1: 1 bp deletion in ﬁrst exon Murphy et al. 2011 causing frameshift and truncated protein (Ma1) Ma2 Sobic.002G302700 SMYD domain SNP in third exon causing premature stop Casto et al. 2019 PhyB Sobic.001G394400 Phytochrome B phyB-1 (ma3 ): SNP in third exon causing Childs et al. 1997; (Ma3) premature stop Yang et al. 2014a Ma4 unknown Unknown NA Quinby et al. 1966 PhyC Sobic.001G087100 Phytochrome C SNPs in exon causing nonsynonymous Yang et al. 2014a (Ma5) mutation SbGhd7 Sobic.006G004400 CCT domain ghd7-1: 5 bp insertion in ﬁrst exon causing Murphy et al. 2014 (Ma6) frameshift and truncated protein Awn Awn1 Sobic.003G421300 ALOG domain Translocation leading to a new promoter Zhou et al. 2021 Glume GC1 Sobic.001G341700 Gc subunit protein gc1-a: 5 bp insertion in ﬁfth exon causing Xie et al. 2022 coverage frameshift and truncated protein Tannin Tan1 Sobic.004G280800 WD40 domain InDels in exon causing frameshift and Wu et al. 2019; Xie content truncated protein et al. 2019 Tan2 Sobic.002G076600 bHLH transcription factor Shattering Sh1 Sobic.001G152901 YABBY domain SC265-like: splicing variant Lin et al. 2012 transcription Tx430-like: SNPs in promoter and intron factor Tx623-like: 2.2-kb deletion Gene loci are based on sorghum bicolor v3.1. SNP single nucleotide polymorphism, InDel insertion and deletion, NA information not available allele with a truncated protein caused by an A to T polysaccharide components were also changed in dw2. mutation in the second exon (Yamaguchi et al. 2016). Phosphoproteomic analysis demonstrated that Dw2 was However, the molecular mechanism of Dw1 remains also involved in regulating lipid signaling and unknown. The Dw2 locus has been detected in many endomembrane trafﬁcking (Oliver et al. 2021). Genome- studies. Through ﬁne-mapping from two recombinant wide selection signal detection found that the Dw2 inbred lines (RIL) populations, Sobic.006G067700 was region has a much higher F value in the improved st ﬁnally conﬁrmed as the candidate gene instead of the accessions than in the ﬁve basic races, indicating that previously reported gene Sobic.006G067600 (Hilley et al. Dw2 was under positive selection in crop improvement 2017). Dw2 encodes a protein kinase belonging to the practice after domestication (Boatwright et al. 2022). AGCVIII subfamily. The recessive dw2 allele carries an Other plant height-related regions were also detected in Indel in the ﬁrst exon, which causes a frameshift and a a genome-wide association study (GWAS), but it is truncated protein. A subsequent study revealed that cell unclear whether the genes are related to domestication. proliferation was repressed in NIL-DDYM (dw2 allele), Another agronomic trait related to shoot architecture resulting in a shortened internode. In addition, mutation is tiller number. Compared with their wild ancestors, of Dw2 caused irregular cell shapes and altered the domesticated and improved crop cultivars exhibit a morphology of vascular bundles. Cell wall great reduction in tiller number due to the beneﬁts of The Author(s) 2022 aBIOTECH close planting. TB1, a basic helix-loop-helix transcription accessions. Haplotype distribution of the D gene was factor negatively regulating tiller number, was ﬁrst found in both African and Asian germplasms. Two cloned in maize, and its orthologous gene in rice or nonfunctional alleles were only distributed in African sorghum plays similar roles (Doebley et al. 1997). A germplasms, which indicated that a nonfunctional higher expression level of SbTB1 observed in the sor- D gene could have been selected at an early stage in ghum phyB-1 mutant revealed the relationship between Africa. tiller development and light signals (Kebrom et al. In another study, the same underlying gene (referred 2006). A population genetic study proved that the to as Dry) in the D locus was also identiﬁed using GWAS SbTB1 region was under strong selection during sor- and map-based cloning (Zhang et al. 2018). The authors ghum domestication. All sorghum cultivars carry the discussed more about the relationship between Dry same haplotype, while variations in the promoter region selection and the origin of domesticated sweet sorghum. of SbTB1 could explain the changes in tiller number Principal component analysis (PCA) based on the between wild and domesticated species (Wu et al. whole-genome resequencing data of 241 sorghum 2022). accessions collected worldwide revealed that the wild, pithy, and juicy accessions were clustered into three Stem juiciness different groups, although there were some exceptions in both the pithy and juicy groups. Dry acts as a master The crop stem parenchyma cells play a role in storing transcription factor that can regulate a series of genes water and nutrients, but become dry or form cavities involved in cell wall biosynthesis and loss of function of surrounded by epidermal cells at the mature stage. the Dry gene in juicy sorghum causes irregular par- Grain sorghum and sweet sorghum exhibit distinct stem enchyma cells and thinner secondary cell walls. A pos- morphology: grain sorghum stems become dry and itive selection signal was detected in the juicy sorghum pithy, while sweet sorghum stems maintain much higher subgroup, which had a signiﬁcantly lower p value than water content and are juicy. This absorbing phenotype the pithy subgroup. Twenty-three haplotypes of the Dry in sorghum has been investigated since last century gene were found in 42 wild sorghum lines with pithy (Swanson and Parker 1931). Early studies suggested stems. Two of them were discovered in 86 landraces that pithy or juicy stems in sorghum were determined exhibiting dry pithy stems, and 112 improved cultivars by a single D locus, and that pithy was dominant to juicy. carried four nonfunctional haplotypes. This variation in It has also been observed that pithy and juicy stems Dry gene haplotype diversity indicates that a bottleneck were closely associated with white and green midribs, effect exists in the Dry gene during sweet sorghum respectively. In 2001, Hart et al. reported that the D lo- domestication. In addition, the Dry locus also exists in cus was cosegregated with the Xtxp97 marker in a collinear genomic regions in other cereal crops, such as sorghum genetic map (Hart et al. 2001). Both later rice, wheat, millet, and maize, indicating that the Dry GWAS and bulked segregant analysis (BSA) have map- locus is an important target in designing crops with ped the D locus, and another study narrowed the D lo- both high grain yield and high stem biomass. cus region with only six genes inside by map-based cloning (Han et al. 2015; Upadhyaya et al. 2022; Zhai Flowering et al. 2014). However, the underlying gene and its role in the origin of sweet sorghum remained obscure until two Sorghum is a short-day C4 grass with photoperiod- 2018 studies. sensitive characteristics that evolved in a tropical, Using an F population derived from a cross between equatorial region. It adapted to long-day environments a dry-stem sorghum SKS and a juicy-stem sorghum after dispersing to high latitudes and temperate regions. MS3B, Fujimoto et al. (2018) ﬁnely mapped the D locus Early ﬂowering was generally selected for grain sor- to an 18.99-kb interval on chromosome 6, and one gene, ghum to ensure reproduction by avoiding drought or Sobic.006G147400 (referred to as the D gene), was low temperature, while other sorghum types, such as conﬁrmed as the candidate gene controlling the juicy sweet sorghum, forage sorghum, and energy sorghum, content in sorghum. The D gene is a NAC domain tran- were selected to have a longer duration of vegetative scription factor that can trigger the programmed cell growth to acquire a higher biomass yield. The diversi- death (PCD) of stem parenchyma cells, which leads to ﬁcation of sorghum ﬂowering time under long-day dry and pithy stems in sorghum. All the investigated conditions indicates that multiple genes could be wild sorghum and dry-stem sorghum cultivars possess a selected to produce photoperiod-insensitive varieties. functional D gene, while six nonfunctional alleles of the Breeders have paid close attention to identifying genes D gene were discovered in juicy-stem sorghum controlling sorghum maturity, and a series of maturity The Author(s) 2022 aBIOTECH loci (named Ma1 to Ma6) have been reported over the was proposed as the underlying gene for Ma5 (Childs last century (Quinby and Karper 1945; Quinby et al. 1997; Yang et al. 2014a). Both PhyB and PhyC have 1966, 1967; Rooney and Aydin 1999). All six loci are been reported to be related to ﬂowering regulation in a dominant in suppressing ﬂowering under long-day light-dependent manner in Arabidopsis and rice. Genetic conditions, and the Ma1, Ma2, Ma3, Ma5, and Ma6 loci evidence revealed that PhyB is epistatic to Ma1 were identiﬁed in these years, which allowed us to (SbPRR37) and Ma6 (SbEhd). PHYB inhibits the obtain a better understanding of their related genetic expression of SbEhd1, which activates the expression of basis. SbCN8 and SbCN12 under long-day conditions. Another Using a BC F population and another F population, sorghum FT gene, SbCN15, is also repressed by PhyB 1 1 2 Ma1 was ﬁne-mapped to an 86-kb interval on chromo- regardless of photoperiod. The underlying gene of Ma2 some 6, and Sb06g014570 (SbPRR37) was conﬁrmed as was ﬁnely mapped as Sobic.002G302700, which encodes the candidate gene (Murphy et al. 2011). SbPRR37 a lysine methyltransferase with a SET and MYND encodes a pseudoresponse regulator, and its expression (SYMD) domain (Casto et al. 2019). It enhances the has two peaks in the morning and evening on long days expression of SbPRR37 and SbCO. A genetic interaction instead of only one morning peak on short days. The between Ma2 and Ma4 was observed. Two recessive higher expression level of SbPRR37 on long days acti- ma2 alleles were discovered in early-ﬂowering sorghum vates the expression of the ﬂoral inhibitor gene CON- lines under long-day conditions. These studies shed STANS (CO) and represses SbEhd1 (Early Heading Date light on the scenario of sorghum diversiﬁcation and 1), which ultimately downregulates FT genes (SbCN8 improvement under human selection for adaptation in and SbCN12) expression. SbCN8 and SbCN12 are ﬂorigen temperate regions. genes that play substantial roles in inducing ﬂowering time (Turck et al. 2008; Yang et al. 2014b). Three non- Awn functional alleles were found in early-ﬂowering acces- sions cultivated in long-day conditions, which indicates The awn is a needle-like structure that extends from the the possible multiple origins of photoperiod-insensitive lemma and is very common in gramineous crops, such sorghum in diversiﬁcation progress when sorghum as wheat, barley, rice, oats, and sorghum (Gu et al. spreads to temperate regions. Another association 2015). There are some advantages to having awns for analysis study of sorghum maturity also identiﬁed the wild species. For example, the awn can prevent insects SbPRR37 gene by using GWAS in a sorghum mini-core and birds from predating the seeds, while a barbed awn collection (Upadhyaya et al. 2013). Multiple variant can help the seeds efﬁciently spread by sticking to alleles of the SbPRR37 genomic sequence from 253 animal furs (Hua et al. 2015; Jagathesan et al. 1961). It landraces and historic sorghum cultivars were found. has also been reported that awns can contribute to yield Some alleles dominantly distributed in a speciﬁc sor- by producing more photosynthate in wheat and barley ghum race or geographic region reveals the selection (Du et al. 2021). In wild wheat, awns can help the seeds history and gene ﬂow of PRR37 when sorghum was germinate by pushing them into the soil. Awns can bend introduced to high latitudes in a new continent by or twist when the surrounding humidity changes and Kaﬁr-1 human activity. For example, prr37 and therefore produce the mechanical force needed to orient Kaﬁr-2 prr37 alleles were mainly distributed in the Kaﬁr the spikelet (Elbaum et al. 2007). However, long cultivar Durra race, and prr37 was dominant in Chinese kaoliang awns cause difﬁculties in harvest, processing, and (Klein et al. 2015). storage. As a result, breeding short-awn or awnless SbGhd7, encoding a protein containing a CCT domain varieties occurs during crop domestication and (CONSTANS, CO-like, and TOC1), was identiﬁed as the improvement. candidate gene in the Ma6 loci (Murphy et al. 2014). Its In addition to the normal seed-bearing spikelets, orthologous gene in rice, GHD7, inhibits the expression sorghum inﬂorescence has sterile pedicellate spikelets. of EHD1, which regulates the expression of Hd3a (FT It has been proven that the sterile spikelets in sorghum, gene in rice) in response to day length. SbGhd7 has a not the awn, can have the capacity for photosynthesis similar expression pattern to SbPRR37 and inhibits the (AuBuchon-Elder et al. 2020). Therefore, sorghum awns expression of SbEhd. Two recessive ghd7 alleles were are likely not a carbon source, although all wild sor- found in photoperiod-insensitive cultivars. The domi- ghum species have long awns. Girma et al. (2019) con- nant alleles of SbGhd7 and SbPRR37 act in an additive ducted a GWAS of the presence or absence of awns fashion to delay ﬂowering under long-day conditions. using 1425 Ethiopian landrace accessions. The GWAS Other studies conﬁrmed that phytochrome B (PhyB)is results revealed a leading peak at 72.6 Mb on chromo- the causal gene in Ma3 loci, and phytochrome C (PhyC) some 3 and identiﬁed eight signiﬁcant SNPs (Girma The Author(s) 2022 aBIOTECH et al. 2019). However, no genetic conﬁrmation was enriching variations in glume coverage in modern sor- performed in this study, and the underlying mechanism ghum accessions. The spikelet morphology of sorghum remains unclear. differs from that of rice and maize. In rice, the glumes A recent study identiﬁed a major gene, Awn1, which degenerated. The revolved hard lemma and palea act as is responsible for awn loss in cultivated sorghum (Zhou glumes to cover the rice seed. In maize cultivars, the et al. 2021). In this study, Zhou et al. ﬁnely mapped the seeds are naked, and the whole ear is covered by bracts awn1 gene through a RIL population constructed from a (Wu et al. 2019). The different spikelet structures cross between the wild sorghum progenitor Sorghum indicate that sorghum could acquire a distinct regula- virgatum (SV) and the improved sorghum cultivar tory network to control glume coverage during Tx623. After narrowing down the interval into a 9.5-kb domestication. region on chromosome 3, sequence comparison showed Recently, Xie et al. (2022) identiﬁed a major gene a large 5.4-kb insertion in the domesticated sorghum located on chromosome 1, GC1, which controls sorghum cultivar Tx623. Only one gene, Sobic.003G42130,was glume coverage using GWAS and positional cloning. Five annotated in this insertion, which was the same candi- main haplotypes were identiﬁed from 482 sorghum date gene in the abovementioned GWAS. accessions, named WT GC1, and mutated gc1-a, gc1-b, Sobic.003G42130 was named awn1 and was proven to gc1-c, and gc1-d. Among them, gc1-b, gc1-c, and gc1-d be derived from an ancestral homologous gene on were rare, while the GC1 (71%) and gc1-a (24%) hap- chromosome 10, Sobic.010G225100, which was referred lotypes were dominant in the evaluated accessions. The to as awn1-10. Awn1 encodes the identical protein with association test demonstrated that GC1 variation was the ALOG domain but recruits a new promoter and has a highly associated with glume coverage instead of yield- higher expression level than awn1-10. Transcriptional related traits (seed length, seed width, and thousand activity assays and yeast two-hybrid assays proved that seed weight). GC1 encodes a protein of 198 amino acids Awn1 is a transcriptional repressor. RNA-seq and DAP- with a Gc-like domain (referred to as GC1-G) and a seq analysis revealed that it can downregulate some predicted transmembrane domain (GC1-T), while gc1-an MADS-box genes involved in ﬂower development and obtains a stop codon at amino acid position 137 but the orthologous genes of DL and LKS2 of rice, leading to reserves the entire GC1-G and GC1-T domains. The a reduction in awn elongation in sorghum. Genomic truncated gc1-a exhibited much lower glume coverage sequence comparison found that this 5.4-kb fragment than WT GC1. Overexpression of GC1 reduced glume on chromosome 10 between SV and Tx623 had more coverage in independent transgenic lines. Interestingly, SNPs than between awn1 and awn1-10 in Tx623, indi- knocking out GC1 increased glume coverage, which was cating that duplication on chromosome 3 could have different from what was observed in gc1-a, indicating occurred after domestication. Tajima’s D test revealed a that the truncated protein could still function during the signiﬁcant selection signal in the neighboring regions of regulation of glume coverage. gc1-a-overexpressing Awn1, and the awnless sorghums had the lowest geno- plants conﬁrmed this hypothesis with signiﬁcantly mic diversity around this region. Awn1 is a largely reduced glume coverage compared with GC1. These effective gene for more than 30% of phenotypic expla- results indicated that both GC1 and the truncated gc1-a nations of awn presence or absence in a natural sor- negatively control glume coverage in sorghum. Overex- ghum population, which could be used in further pressing or knocking out the orthologous gene of GC1 in awnless sorghum breeding. Homologs of Awn1 could be millet also supported this conclusion. further exploited in other cereals, and it is unclear Further study conﬁrmed that the truncated C-termi- whether it also experienced similar parallel selection. nus of GC1 caused a higher protein accumulation in vivo, which inhibited glume cell proliferation by Glume coverage downregulating cyclin-CDK-related genes. An interact- ing phospholipase protein, SbpPLAII-1, identiﬁed by Wild sorghum has a pair of tenacious glumes that cover immunoprecipitation-mass spectrometry (IP-MS), pro- the seed, which can protect the seed from being infected moted the expression of cyclin-CDK-related genes and by fungi, birds, and insects in the natural environment. longer glumes. SbpPLAII-1 could be degraded when GC1 However, it caused a huge obstacle for threshing during or gc1-a was accumulated. The more stable gc1-a sorghum domestication. In agricultural practice, seeds accelerated this degradation process compared with tightly covered by glumes pose difﬁculties for modern GC1. These results demonstrated that naturally trun- automated planting, threshing, and processing cated variations of GC1 contributed to lower glume (Adeyanju et al. 2015). As a result, farmers favor sor- coverage in sorghum by degrading SbpPLAII-1 and ghum grains with low glume coverage, which induces downregulating the expression of cell division-related The Author(s) 2022 aBIOTECH genes. Tajima’s D test showed a signiﬁcant selection residence time for sparrow feeding. It is known that the signal in landraces and improved cultivars with low WD40 protein can form a ternary complex by interact- glume coverage. In addition, the nucleotide diversity in ing with MYB and basic helix-loop-helix (bHLH) proteins the exon 5 and 3’UTR of GC1 was also signiﬁcantly to control multiple biological processes (Ramsay and reduced in the naked landraces and improved lines Glover 2005). Further studies revealed that tan1-a/b compared with wild sorghum. The geographic distri- likely promoted more fatty acid-derived volatiles than butions of ﬁve different haplotypes in this study also Tan1, possibly by repressing the expression of SbGL2,a indicated that the Sahelian zone is a domestication key negative regulator of fatty acid biosynthesis. center of sorghum. Wu et al. (2019) reported that Tan1 and another gene, Tannin2 (Tan2), were both involved in sorghum Tannin content tannin content regulation. It was identiﬁed by QTL mapping and a combined GWAS. Using the different bird Proanthocyanidins (PAs) are condensed tannins and are damage levels as phenotype data, ﬁve signiﬁcant loci products of the ﬂavonoid biosynthesis pathway. They were identiﬁed from QTL mapping of a RIL population have astringent properties and are present in sorghum derived from a cross between P898012 and Tx430. grains but absent in other main cereal crops, such as Three of them were related to plant height, but only two corn, wheat, and rice (Wu et al. 2012). Tannin evalua- signiﬁcant loci located on chromosomes 4 and 2 were tion of 11,577 cultivated sorghum accessions showed left when using the tannin presence as the phenotype that tannin and non-tannin types were present in data. These two loci were also identiﬁed in the GWAS approximately equal proportions (45% and 55%, using tannin content as the input data. The mapping respectively) (Wu et al. 2019). However, it is unclear region on chromosome 4 contained Tannin1, which has why domesticated sorghum still preserved these bitter been proven to regulate tannin presence in sorghum chemicals under human selection. An early study grains in a previous study (Wu et al. 2012), and the reported that the presence of tannin in sorghum grain allele carrying a 1-base pair insertion (referred to as was regulated by two genes (B1 and B2) (Smith and tan1-a) in the coding sequence caused the non-tannin Frederiksen 2000). Wu et al. (2012) identiﬁed the grains in Tx430. After sequence variation analysis, Tannin1 (Tan1) gene involved in condensed tannins Sobic.002G076600 was considered the candidate gene of biosynthesis in sorghum. In 2019, two studies identiﬁed Tan2. This was also conﬁrmed by complementing the the same locus related to the presence of tannin in Arabidopsis tt8 mutant with modiﬁed seed pigmentation sorghum and shed light on the underlying regulatory (Nesi et al. 2000). A 5-bp insertion in Tan2 (encoding a mechanism between tannin content and bird feeding protein with bHLH domain) caused a frameshift in behavior. Tx430 and was denoted as tan2-a. Xie et al. (2019) ﬁrst collected phenotypic data by Tannin and non-tannin plants are segregated at a evaluating bird-preference and bird-avoidance charac- ratio of 1:3 in the RIL population. These results indi- teristics from the ﬁeld and identiﬁed a signiﬁcant SNP cated that Tan1 and Tan2 were the underlying genes of within the Tan1 gene involved in ﬂavonoid and PA the B1 and B2 loci, respectively, and sorghum grain biosynthesis by GWAS. This locus was stably detected tannin was present only when both genes were domi- regardless of the phenotype of tannin content or by bird nant. The recessive alleles, tan1-b, tan1-c, and tan2-b, damage levels under different populations and ﬁeld tan2-c, of each gene were discovered from 88 non-tan- conditions, indicating that there was a relationship nin accessions, with tan1-b and tan2-b at a low fre- between tannin content and the level of bird damage. quency. tan1-a was mainly distributed in East and West This was proven because bird-preference sorghum Africa, while tan2-a dominated in South and West accessions had signiﬁcantly reduced levels of metabo- Africa. In addition, tan1-c and tan2-c were mainly pre- lites involved in anthocyanin and PA biosynthesis. Two sent in South and East Africa, and no tan2-a allele was mutated alleles, tan1-a and tan1-b, with no detected observed in East Africa. These results indicate that non- tannins were associated with a much more severe bird tannin sorghum could have multiple domestication damage phenotype compared with the wild-type Tan- origins. Further study conﬁrmed that tannin sorghum nin1 (Tan1). Sparrow feeding experiments demon- had a higher proportion in East and South Africa where strated that sparrows fed on fewer seeds coated with bird damage was severe, while non-tannin sorghum malvidin or PA than untreated seeds. On the other hand, dominated in West Africa where bird threats were mild. bird-preference seeds with tan1-a/b alleles produced Interestingly, the geographic distribution of tannin sor- more fragrant volatile organic compounds, such as ghum was also connected to human TAS2R variants. It 1-octen-3-ol and hexanal, which caused a longer was assumed that humans carrying a TAS2R haplotype The Author(s) 2022 aBIOTECH Tx623-like were insensitive to bitter tastes, thus contributing to the Sh1 , respectively (Wu et al. 2022). Interestingly, selection of tannin sorghum to address local severe bird the syntenic region harboring orthologous genes related threats in East and South Africa. In contrast, humans to the non-shattering phenotype in rice and maize was carrying another TAS2R haplotype could perceive a also under positive selection, which illustrates that the bitter taste and prefer non-tannin sorghum in West orthologous genomic region of Sh1 underwent parallel Africa. The interactions among plants, humans, and the selection in different cereal lineages. environment demonstrate the complexity of tannin SpWRKY, identiﬁed from a wild sorghum species, content domestication in sorghum. Sorghum propinquum, is also a major gene for sorghum seed shattering (Tang et al. 2013). Compared to the non- Seed shattering shattering allele SbWRKY, SpWRKY has a longer trans- lated protein since it recruits a new start codon. How- Loss of seed shattering is considered a hallmark of crop ever, it seems that SbWRKY is not related to domestication (Li et al. 2006). Wild ancestors of modern domestication. It is more likely that Sorghum propin- crops disperse their seeds by forming an abscission quum keeps the seed shattering by obtaining a func- layer between the seed and pedicel, which causes seed tional SpWRKY from a shared common ancestor with shattering and helps their seeds fall off into the soil in a Sorghum bicolor. Intriguingly, the expression of SpWRKY timely manner and propagate efﬁciently. However, seed in non-shattering RTx430 restored the shattering phe- shattering is an unfavorable phenotype for farmers, notype. Regardless, the relationships and molecular since it results in great yield losses and causes difﬁ- mechanisms between the two genes remain largely culties in harvesting. As a result, non-shattering variants unknown and must be further elucidated. were selected during domestication among most crops. Sh1 is the major gene controlling sorghum seed shattering (Lin et al. 2012). It is cloned using a large F CONCLUSIONS AND PERSPECTIVES population containing approximately 15,000 individuals derived from a cross of a wild sorghum Sorghum vir- Crop domestication is a protracted process that entails gatum (SV) and a domesticated cultivar Tx430. A YABBY the early selection of wild progenitors, subsequent domain transcription factor was identiﬁed as the can- diversiﬁcation when the landrace spreads to a new didate gene of Sh1 loci. Sequence variation in Sh1 environment, and modern improvement breeding. In revealed four main haplotypes, including the wild hap- this review, we discussed the origin and classiﬁcation of SV-like lotype SV-like Sh1 (Sh1 ) and three domesticated ﬁve basic cultivated breeds of sorghum. Genomic SC265-like haplotypes, SC265-like Sh1 (Sh1 ), Tx430-like information reveals that there is no obvious domesti- Tx430-like Tx623-like Sh1 (Sh1 ), and Tx623-like Sh1 (Sh1 ). cation bottleneck in sorghum, which differs from other SV-like Tx430-like Compared to Sh1 , Sh1 has four causal main crops. We summarized key genes that have changes in the promoter and the second intron, which recently been reported to be involved in sorghum leads to a lower expression level. Variations in domestication and elucidated their genetic molecular Tx623-like SC265-like Sh1 and Sh1 cause frameshift muta- mechanisms. The underlying genes of these agronomic tions, resulting in truncated proteins lacking the zinc traits were discussed in detail, and the genomic foot- ﬁnger and YABBY domains. The proportion of these prints of these genes give us a better understanding of three non-shattering haplotypes varies in domesticated how plants can achieve ideal traits between the envi- sorghum races. For example, in the investigated sor- ronment and human activity during their evolutionary Tx430-like ghum accessions, Sh1 is prevalent in the cau- process. datum race, while all durra races, most guinea races, Cereal domestication started in the Neolithic Age and approximately half of bicolor races carry approximately 10,000 years ago. During the evolution- SC265-like Tx623-like Sh1 . The other haplotype, Sh1 ,is ary process of plants, multiple agronomic traits were mainly comprised of kaﬁr and bicolor races and is altered that beneﬁted humans during parallel selection widely distributed in South and East Africa. These across major crops, which is known as domestication results indicate that non-shattering sorghum could have syndrome (Gepts 2014; Stetter et al. 2017). The genes been simultaneously domesticated in different regions that occur in parallel selection always occupy few but from local relative wild ancestors. Another study found important signaling pathway positions. Loss or gain of that the three wild sorghum accessions SL129, SL12, function in these paralleled selected genes are con- and SL32, collected from Kenya, Nigeria, and Tanzania, served in related crop species despite different muta- respectively, could be the ancestors of the non-shatter- tion forms (Lenser and Theissen 2013). Recently, an Tx430-like SC265-like ing haplotypes Sh1 , Sh1 , and increase in our knowledge about key genes underlying The Author(s) 2022 aBIOTECH (32201780) and the Agricultural Breeding Program in NingXia domestication-related traits has been identiﬁed in rice, Province (2019NYYZ04 and 2019BBF02022-05). maize, and wheat (Fernie and Yan 2019), which could inspire research of sorghum domestication. For exam- Data availability Data sharing is not applicable to this article, as ple, the only identiﬁed major gene, SbTB1, controlling no datasets were generated or analyzed during the current study. tiller number in sorghum, is the ortholog of well-known Declarations TB1 in maize (Doebley et al. 1997). However, this does not occur in some homologs of those reported distin- Conﬂict of interest The authors declare no conﬂicts of interest. guished genes due to distinct selection pressure. Millet Author Qi Xie was not involved in the journal’s review of the SiGC1, the ortholog to sorghum GC1, did not exhibit a manuscript. parallel section in naked grains since it already had thin glumes and easy-threshing grains (Xie et al. 2022). It is Open Access This article is licensed under a Creative Commons noteworthy that these key domesticated genes are also Attribution 4.0 International License, which permits use, sharing, located in simple regulatory pathways and have mini- adaptation, distribution and reproduction in any medium or for- mal pleiotropic effects, which can prevent additional mat, as long as you give appropriate credit to the original side effects on other important agronomic traits, such as author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other the ﬂowering time pathway (Turck et al. 2008). third party material in this article are included in the article’s One cost of crop domestication is mutation load, Creative Commons licence, unless indicated otherwise in a credit which refers to the increase in deleterious mutations in line to the material. If material is not included in the article’s the genome (Gaut et al. 2018). Domestication also Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will caused a loss of rare or elite alleles that could resist need to obtain permission directly from the copyright holder. To biotic or abiotic stress. Interestingly, domesticated crops view a copy of this licence, visit http://creativecommons.org/ or animals can reacquire wild-like traits, which is called licenses/by/4.0/. the de-domestication process (Wu et al. 2021). In sor- ghum, the effects of mutation load can be mitigated by occasional hybridization between different sorghum References accessions (Brown 2019; Smith et al. 2019). A modern Adeyanju A, Perumal R, Tesso T (2015) Genetic analysis of understanding of the molecular mechanisms underlying threshability in grain sorghum [Sorghum bicolor (L.) domestication-related genes and the site-directed Moench]. 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aBIOTECH – Springer Journals
Published: Mar 1, 2023
Keywords: Domestication; Genetic basis; Molecular mechanism; Genes; Sorghum
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