Genetic Structure and Molecular Mechanisms Underlying the Formation of Tassel, Anther, and Pollen in the Male Inflorescence of Maize (Zea mays L.)
Abstract
:1. Introduction
2. Cellular Developmental Process of Maize Male Inflorescence
3. Genes and the Molecular Regulation Mechanisms of Male Inflorescence Development and Tassel Morphology
3.1. Meristem Activity and Maintenance
3.2. Axillary Meristem Initiation and Formation in the Reproductive Phase
3.3. Regulation of Meristem Fate
3.4. Regulation of TBA
4. Genetic Basis of Tassel Traits Revealed by Quantitative Genetics Methodologies
5. Application of the Quantitative Genetic Variation Regulating Tassel Traits in Maize Breeding
6. The Cloned Maize GMS Genes and Their Roles in Anther and Pollen Development
Categories | Gene Names | Encoded Proteins | Expression Stages | Molecular Functions | Orthologs | References |
---|---|---|---|---|---|---|
Transcription Factors | OCL4 | HD-ZIP IV transcription factor | S5 | Relates to anther wall development in early stage | - | [152] |
ZmTGA9-1 | bZIP family transcription factor | S5 | Involve in the Ubisch bodies and cuticle formation of anther wall | AtTGA9 | [68,150,153] | |
ZmTGA9-2 | S5 | |||||
ZmTGA9-3 | S5–S6 | |||||
ZmTGA10 | S5 | Controls anther dehiscence | OsTGA10, AtTGA10 | [68,153,154] | ||
ZmMs32 | bHLH transcription factor | S6 | Controls periclinal division and tapetum differentiation | OsUDT1, AtDYT1 | [155,156,157] | |
ZmbHLH122 | S5–6 and S8 | Relate to the formation of anther cuticle and Ubisch bodies | OsEAT1 | [68] | ||
ZmbHLH51 | S6 to S9 | OsTDR, AtAMS | [68,158] | |||
ZmMs23 | S5 to S8 | Controls tapetal specification and maturation | OsTIP2/ bHLH142 | [159,160,161] | ||
ZmMs9 | R2/R3 MYB transcription factor | S6 and S9 | The control point for the entry into meiosis | OsTDF1, AtTDF1 | [162,163] | |
ZmMYB33-1 | MYB transcription factor | S7 and S10 | Involve in the Ubisch bodies and cuticle formation of anther wall and pollen development | OsGAMYB, AtMYB33/65 | [68,164] | |
ZmMYB33-2 | S7 and S10 | OsGAMYB, AtMYB33/65 | ||||
ZmMYB80 | S8b-S9 | Involves in the Ubisch bodies formation and pollen development | OsMYB80, AtMYB80 | [68,165,166] | ||
ZmPHD11 | PHD transcription factor | S8a-S8b | Involves in the Ubisch bodies and cuticle formation of anther wall | OsTIP3, AtMMD1 | [68,167,168] | |
ZmMs7 | S8b-S9 | Involves in tapetum development and pollen exine formation | OsPTC1, AtMs1 | [169,170] | ||
IG1 | LBD transcription factor | S9 | Involves in leaf and embryo sac development | OsIG1, AS2 | [171] | |
ZmLBD27 | S7–S8b, S11–S12 | Important for viable pollen formation | AtLBD10 | [68,172] | ||
ZmLBD10 | S11–S12 | AtLBD10 | ||||
Lipid Metabolism | ZmMs33 | Glycerol-3-phosphate acyltransferase (GPAT) | S6 | Plays important roles in anther cuticle, exine and Ubisch bodies formation | OsGPAT3 | [173,174,175] |
ZmMs26 | Cytochrome P450 monooxygenase | S6 and S9 | Regulates pollen exine formation | OsCYP704B2, AtCYP704B1 | [176] | |
ZmMs10/ APV1 | P450 subfamily protein | S6 and S9 | Specifically expresses in the tapetum and involve in the hydroxylation of lauric acid | OsCYP704B2, AtCYP704B1 | [177] | |
ZmMs30 | GDSL lipase | S7–S8 | Regulates exine formation | - | [178] | |
Zmms44 | Lipid transfer protein | S7–8 | Involves in postmeiotic tapetum secretion of proteins from tapetal cells into locule | - | [179] | |
IPE1/ZmMs20 | Putative glucose-methanolcholine oxidoreductase | S8b–S9 | Controls anther cuticle and exine development | OsNP1 | [180,181,182] | |
IPE2 | GDSL lipase | S8b–S9 | Essential for anther cuticle and exine formation | - | [183] | |
ZmMs6021/ ZmMs25/ ZmFAR1 | Acyl-coenzyme A (CoA)-acyl carrier protein | S9 | Affects anther cuticle and Ubisch body formation as well as microspore development | OsDPW, AtMs2 | [184,185,186] | |
ZmMs45 | Strictosidine synthase | S9 | Involves in pollen wall initiation after tetrad stage | OsSTRL2, AtLAP3 | [42,187] | |
ZmMs2/ ZmABCG26 | ABCG transporter | S9 | Transports lipid molecules to exine | OsABCG15, AtABCG26 | [185,188] | |
AmACOS5-2 | Acyl-CoA Synthetase 5 | - | Play a role in sporopollenin synthesis | OsACOS12, AtACOS5 | [150,189,190,191] | |
ZmDFR1 | Dihydroflavonol-4-reductase 1 | OsTKPR1, AtTKPR1 | [150,192,193] | |||
ZmDFR2 | Dihydroflavonoid reductase 2 | OsTKPR1, AtTKPR1 | ||||
Polysaccharide Metabolism | ZmMs8 | β-1,3-galactosyltransferases | S7–S8 | Affects the epidermal and tapetal cells of maize anthers and meiosis at dyad stage | AtKNS4 | [194,195,196] |
Other Processes | ZmMs22/ MSCA1 | Plant-specific CC-type GRX | S5 | Controls the redox state and the initiation of archesporial cells | OsMIL1, AtROXY1/2 | [197,198,199] |
MAC1 | Small secreted protein | S6 | Suppresses excess AR proliferation, triggers periclinal division of subepidermal cells | OsTDL1A | [200] |
6.1. GMS Genes in Phase I (Archesporial Cell Specification)
6.2. GMS Genes in Phase II (Anther Somatic Cell Division)
6.3. GMS Genes in Phase III (Tapetum Development and PMC Formation)
6.4. GMS Genes in Phase IV (Mature Pollen Formation and Anther Dehiscence)
7. Application of GMS Genes in Maize Heterosis Utilization
8. Conclusions and Perspectives
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Types | Gene Names | Gene IDs (Zm00001d) | Positions | Annotations | References |
---|---|---|---|---|---|
Genes regulating meristem activity | CT2 | 027886 | Chr1: 16721214–16732176 | Subunit (Gα) of a heterotrimeric GTP binding protein | [70] |
FEA2 | 051012 | Chr4: 136764371–136769212 | LRR receptor-like protein | [71] | |
FEA3 | 040130 | Chr3: 28709631–28715222 | LRR receptor | [72] | |
FEA4 | 037317 | Chr6: 120722612–120728273 | bZIP transcription factor | [73] | |
TD1 | 014793 | Chr5: 63455339–63461620 | LRR receptor-like kinase | [74] | |
TVT1-R | 045192 | Chr9: 15719302–15730427 | Ribonucleotide reductase | [75] | |
ZmGB1 | 033422 | Chr1: 262590898–262600232 | Subunit (Gβ) of a heterotrimeric GTP binding protein | [76] | |
ZmWUS1 | 001948 | Chr2: 3416796–3418004 | Homeodomain transcription factor | [77] | |
ZmWUS2 | 026537 | Chr10: 147855536–147856873 | Homeodomain transcription factor | [77] | |
Genes controlling BM development | BA1 | 042989 | Chr3: 186013129–186016764 | bHLH transcription factor | [78,79] |
BA2 | 003897 | Chr2: 65741213–65756966 | Nucleoprotein | [64] | |
BIF1 | 008749 | Chr8: 18950258–18955333 | Aux/IAA protein | [80,81] | |
BIF2 | 031068 | Chr1: 175806351–175810932 | Serine/threonine protein kinase | [81,82,83,84] | |
BIF4 | 037691 | Chr6: 134087331–134094170 | Aux/IAA protein | [81] | |
KN1 | 033859 | Chr1: 276071835–276082742 | KNOTTED1-like homeobox (KNOX) transcription factor | [85,86,87] | |
LG2 | 042777 | Chr3: 179386227–179397947 | bZIP transcription factor | [88] | |
QDtbn1 | 053358 | Chr4: 227482692–227483909 | Kelch repeat-containing F-box protein | [89] | |
RTE | 030656 | Chr1: 151219729–151227321 | Membrane-localized boron efflux transporter | [90] | |
SPI1 | 044069 | Chr3: 218285795–218290961 | Flavin monooxygenase | [91] | |
TLS1 | 032461 | Chr1: 227447816–227454579 | Boron channel protein | [92] | |
TSH4 | 020941 | Chr7: 137272100–137278639 | SBP-box transcription factor | [93] | |
TU1 | 052180 | Chr4: 181855808–181865542 | MADS box transcription factor | [94] | |
UB2 | 031451 | Chr1: 190381366–190388089 | SBP-box transcription factor | [95] | |
UB3 | 052890 | Chr4: 203609847–203617018 | SBP-box transcription factor | [95,96] | |
VT2 | 008700 | Chr8: 17393223–17400365 | Grass-specific tryptophan aminotransferase | [97] | |
ZFL1 | 026231 | Chr10: 141560362–141566267 | FLO/LFY homolog | [98] | |
ZFL2 | 002449 | Chr2: 12912591–12918568 | FLO/LFY homolog | [98] | |
Genes controlling meristem fate | BD1 | 022488 | Chr7: 178604458–178608405 | ERF transcription factor | [99] |
IDS1 | 034629 | Chr1: 298421359–298428550 | AP2 transcription factor | [100,101] | |
NA1 | 042843 | Chr3: 181819965–181824489 | 5α-steroid reductase | [102] | |
RA1 | 020430 | Chr7: 113570910–113574437 | Cys2-His2 zinc-finger transcription factor | [103] | |
RA2 | 039694 | Chr3: 12156780–12160565 | LOB-domain transcription factor | [104] | |
RA3 | 022193 | Chr7: 172483459–172490694 | Trehalose-6phosphate phosphatase | [105] | |
REL2 | 024523 | Chr10: 75992328–76004412 | Transcriptional co-repressor similar to TOPLESS protein | [106] | |
Si3 | 004130 | Chr2: 85360621–85369941 | Putative transcriptional regulator | [107] | |
SID1 | 019230 | Chr7: 23052961–23067089 | AP2 transcription factor | [101] | |
TS1 | 003533 | Chr2: 47103687–47110872 | Lipoxygenase | [6] | |
TS2 | 028806 | Chr1: 46953827–46958171 | Short-chain alcohol dehydrogenase | [108] | |
MicroRNAs mediated inflorescence development | CG1 | - * | Chr3: 7773052–7777625 | MiRNA156 | [109] |
FZT | 027412 | Chr1: 4722956–4738332 | DICER-LIKE1 | [110] | |
TS4 | - * | Chr3: 144916511–144920220 | MiRNA172 | [111] | |
Genes controlling tassel branch angel | BAD1 | 005737 | Chr2: 185420859–185424689 | TCP transcription factor | [112] |
BAF1 | 045427 | Chr9: 21784850–21788875 | AT hook transcription factor | [113] | |
LG1 | 002005 | Chr2: 4229354–4236035 | SBP-box transcription factor | [114] | |
TSH1 | 039113 | Chr6: 170246513–170250985 | GATA zinc-finger protein | [115] |
BMS System | Gene Names | Elements | References | ||||
---|---|---|---|---|---|---|---|
SPT | ZmMs45 | pZmMs5126::ZmMs45 | pPG47::Bt1:ZmAA | 35SEN-pLTP2::DsRed2 | [42] | ||
MCS | ZmMs7 | pZmMs7::ZmMs7 | pPG47::Bt1:ZmAA | pLTP2::mCherry | p35S::Bar | pZm13::Dam | [169,174,178] |
MCS | ZmMs30 | PZmMs30::ZmMs30 | pPG47::Bt1:ZmAA | pLTP2::mCherry | p35S::Bar | [169,174,178] | |
MCS | ZmMs33 | PZmMs33::ZmMs33 | pPG47::Bt1:ZmAA | pLTP2::mCherry | p35S::Bar | pZm13::Dam | [169,174,178] |
DGMS | ZmMs7 | PZmMs5126::ZmMs7 | pLTP2::mCherry | p35S::Bar | [170] | ||
DGMS | ZmMs44 | pZmMs44::ZmMs44 miRNA | pPG47::Bt1:ZmAA | 35SEN-pLTP2::DsRed2 | [179] |
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Wang, Y.; Bao, J.; Wei, X.; Wu, S.; Fang, C.; Li, Z.; Qi, Y.; Gao, Y.; Dong, Z.; Wan, X. Genetic Structure and Molecular Mechanisms Underlying the Formation of Tassel, Anther, and Pollen in the Male Inflorescence of Maize (Zea mays L.). Cells 2022, 11, 1753. https://doi.org/10.3390/cells11111753
Wang Y, Bao J, Wei X, Wu S, Fang C, Li Z, Qi Y, Gao Y, Dong Z, Wan X. Genetic Structure and Molecular Mechanisms Underlying the Formation of Tassel, Anther, and Pollen in the Male Inflorescence of Maize (Zea mays L.). Cells. 2022; 11(11):1753. https://doi.org/10.3390/cells11111753
Chicago/Turabian StyleWang, Yanbo, Jianxi Bao, Xun Wei, Suowei Wu, Chaowei Fang, Ziwen Li, Yuchen Qi, Yuexin Gao, Zhenying Dong, and Xiangyuan Wan. 2022. "Genetic Structure and Molecular Mechanisms Underlying the Formation of Tassel, Anther, and Pollen in the Male Inflorescence of Maize (Zea mays L.)" Cells 11, no. 11: 1753. https://doi.org/10.3390/cells11111753