Rice Science ›› 2023, Vol. 30 ›› Issue (5): 379-404.DOI: 10.1016/j.rsci.2023.03.014
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Lu Xuedan1,2, Li Fan1, Xiao Yunhua1,2, Wang Feng1,2, Zhang Guilian1,2, Deng Huabing1,2, Tang Wenbang3,4(
)
Received:2022-07-05
Accepted:2023-03-08
Online:2023-09-28
Published:2023-08-14
Contact:
Tang Wenbang (Lu Xuedan, Li Fan, Xiao Yunhua, Wang Feng, Zhang Guilian, Deng Huabing, Tang Wenbang. Grain Shape Genes: Shaping the Future of Rice Breeding[J]. Rice Science, 2023, 30(5): 379-404.
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| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| RGA1 | Os05g0333200 | Gα subunit | + | None | / | + | Proliferation | Oki et al, |
| GS3 | Os03g0407400 | Atypical Gγ subunit | − | + | − | − | Proliferation and elongation | Fan et al, |
| DEP1 | Os09g0441900 | Atypical Gγ subunit | + | / | / | / | / | Huang et al, |
| RGB1 | Os03g0669100 | Gβ subunit | + | / | / | / | Proliferation | Utsunomiya et al, |
| GGC2 | Os08g0456600 | Atypical Gγ subunit | + | / | / | / | / | Sun et al, |
| RGG1 | Os03g0635100 | Typical Gγ subunit | − | − | / | − | Proliferation | Sun et al, |
| RGG2 | Os02g0137900 | Typical Gγ subunit | − | − | − | − | Expansion | Sun et al, |
| OsMADS1/OsLG3b | Os03g0215400 | Transcription factor downstream of GS3 and DEP1 | + | / | + | + | Proliferation | Liu et al, |
Table 1. Main regulators in G protein signaling for rice grain shape.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| RGA1 | Os05g0333200 | Gα subunit | + | None | / | + | Proliferation | Oki et al, |
| GS3 | Os03g0407400 | Atypical Gγ subunit | − | + | − | − | Proliferation and elongation | Fan et al, |
| DEP1 | Os09g0441900 | Atypical Gγ subunit | + | / | / | / | / | Huang et al, |
| RGB1 | Os03g0669100 | Gβ subunit | + | / | / | / | Proliferation | Utsunomiya et al, |
| GGC2 | Os08g0456600 | Atypical Gγ subunit | + | / | / | / | / | Sun et al, |
| RGG1 | Os03g0635100 | Typical Gγ subunit | − | − | / | − | Proliferation | Sun et al, |
| RGG2 | Os02g0137900 | Typical Gγ subunit | − | − | − | − | Expansion | Sun et al, |
| OsMADS1/OsLG3b | Os03g0215400 | Transcription factor downstream of GS3 and DEP1 | + | / | + | + | Proliferation | Liu et al, |
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| GW2 | Os02g0244100 | RING-type E3 ubiquitin ligase | − | − | − | − | Proliferation and expansion | Song et al, |
| HGW | Os06g0160400 | Ubiquitin-associated domain protein | None | + | + | / | Division and elongation | Li et al, |
| WTG1/ OsOTUB1 | Os08g0537800 | Deubiquitinating enzyme | + | − | − | − | Proliferation and expansion | Huang et al, et al, |
| OsUBP15/LG1 | Os02g0244300 | Deubiquitinating enzyme | + | + | + | + | Proliferation | Shi et al, |
| bZIP47 | Os06g0265400 | bZIP transcription factor | + | − | / | − | Proliferation | Hao et al, |
| OsUBC13 | Os01g0673600 | E2 ubiquitin-conjugating protein | / | + | / | + | / | Hao et al, |
| WG1/OsGRX8 | Os02g0512400 | Glutaredoxin protein/target of GW2 | − | + | / | + | Proliferation | Hao et al, |
Table 2. Main regulators in ubiquitination-related pathway for rice grain shape.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| GW2 | Os02g0244100 | RING-type E3 ubiquitin ligase | − | − | − | − | Proliferation and expansion | Song et al, |
| HGW | Os06g0160400 | Ubiquitin-associated domain protein | None | + | + | / | Division and elongation | Li et al, |
| WTG1/ OsOTUB1 | Os08g0537800 | Deubiquitinating enzyme | + | − | − | − | Proliferation and expansion | Huang et al, et al, |
| OsUBP15/LG1 | Os02g0244300 | Deubiquitinating enzyme | + | + | + | + | Proliferation | Shi et al, |
| bZIP47 | Os06g0265400 | bZIP transcription factor | + | − | / | − | Proliferation | Hao et al, |
| OsUBC13 | Os01g0673600 | E2 ubiquitin-conjugating protein | / | + | / | + | / | Hao et al, |
| WG1/OsGRX8 | Os02g0512400 | Glutaredoxin protein/target of GW2 | − | + | / | + | Proliferation | Hao et al, |
Fig. 1. Control of grain shape by ubiquitination-related pathway. GW2, a RING protein with E3 ubiquitin (Ub) ligase activity, interacts and catalyzes the ubiquitination of EXPLA1 and WG1/OsGRX8. EXPLA1 is a cell wall-loosening protein that increases cell expansion, while WG1/OsGRX8 acts as an adaptor protein to recruit the transcriptional co-repressor ASP1 to repress the transcription activity of OsbZIP47. OsbZIP47 limits grain growth by inhibiting cell proliferation. The deubiquitinase WTG1/OsTUB1 forms complex with E2 conjugating enzyme OsUBC13 to regulate grain width, maybe through promoting the ubiquitination-dependent proteasomal degradation of OsSPL14, and thus longitudinally increases cell length and transversely decreases cell width. Another deubiquitinase OsUBP15 positively regulates cell proliferation to determine grain shape. Moreover, a novel plant-specific ubiquitin-associated domain protein HGW (heading and grain weight) promotes latitudinal cell division to play a role in grain shape determination. Regular arrows indicate positive regulation, while block arrows indicate negative regulation.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| OsMKK4 | Os02g0787300 | MAPK kinase | + | + | / | + | Proliferation | Duan et al, |
| OsMAPK6 | Os06g0154500 | MAPK | + | + | / | + | Proliferation | Liu S Y et al, |
| OsWRKY53 | Os05g0343400 | Substrate of OsMAPK6 | + | + | / | / | Expansion | Tian et al, |
| GSN1/OsMKP1 | Os05g0115800 | MAPK phosphatase | − | − | / | − | Proliferation | Guo et al, |
| OsMKKK10 | Os04g0559800 | MAPK kinase kinase | + | + | / | + | Proliferation | Xu et al, |
Table 3. Main regulators in mitogen-activated protein kinase (MAPK) signaling pathway for rice grain shape.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| OsMKK4 | Os02g0787300 | MAPK kinase | + | + | / | + | Proliferation | Duan et al, |
| OsMAPK6 | Os06g0154500 | MAPK | + | + | / | + | Proliferation | Liu S Y et al, |
| OsWRKY53 | Os05g0343400 | Substrate of OsMAPK6 | + | + | / | / | Expansion | Tian et al, |
| GSN1/OsMKP1 | Os05g0115800 | MAPK phosphatase | − | − | / | − | Proliferation | Guo et al, |
| OsMKKK10 | Os04g0559800 | MAPK kinase kinase | + | + | / | + | Proliferation | Xu et al, |
Fig. 2. Control of grain shape by brassinosteroid (BR) and mitogen-activated protein kinase (MAPK) signaling pathway. The rate limiting enzymes in BR synthesis, including SLG, D2/CYP90D2, DWARF11, DWARF4 and brd1/OsBR6ox/OsDWARF, are involved in grain shape determination through regulation of BR homeostasis. The BR signal is perceived by OsBRI1 and its co-receptor OsBAK1 and transduced to OsBSK3, which phosphorylates an unidentified phosphatase and further represses OsGSK2/OsSK22 and OsGSK3. OsGSK2 and OsGSK3 repress BR signaling by negatively regulating the transcription factors including OsBZR1, DLT, GL2/GS2/OsGRF4, OsWRKY53 and OFPs. OFPs repress the transcription activity of GS9. A protein phosphatase GL3.1/OsPPKL1 dephosphorylates but stabilizes OsGSK3, leading to accumulation of phosphorylated OsBZR1, which cannot activate BR-induced genes and thus suppressing BR signaling. GL3.1/OsPPKL1 also induces the phosphorylation of OsGF14b, which inhibits OsBZR1 to translocate to nucleus. OsGSK2 phosphorylates OsMKK4 to suppress OsMAPK6 activity, while the phosphorylation of OsWRKY53 by GSK2 lowers OsWRKY53 protein stability to regulate grain shape. GSN1/OsMKP1 inactivates OsMAPK6 via dephosphorylation and thus negatively regulates grain length and width formation. Regular arrows indicate positive regulation, while block arrows indicate negative regulation.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| GW8/OsSPL16 | Os08g0531600 | Target of miR156 | − | + | / | − | Proliferation and elongation | Wang et al, |
| GLW7/OsSPL13 | Os07g0505200 | Transcription factor, target of miR156 | + | None | + | + | Expansion | Si et al, |
| OsmiR396e | Os04g0674500 | miRNA396 | − | − | − | − | Elongation and expansion | Miao et al, |
| OsmiR396f | Os02g0829000 | miRNA396 | − | − | − | − | Elongation and expansion | Miao et al, |
| SPL4 | Os02g0829000 | Target of miR156 | − | − | + | − | Elongation and division | Hu et al, |
| OsmiR167a | miRNA167 | + | / | / | + | Elongation | Qiao et al, | |
| OsmiR529a | miRNA529 | + | − | / | − | / | Yan et al, | |
| OsmiR408 | miRNA408 | + | + | / | + | Elongation | Yang et al, | |
Table 4. Main regulators in microRNA process for rice grain shape.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| GW8/OsSPL16 | Os08g0531600 | Target of miR156 | − | + | / | − | Proliferation and elongation | Wang et al, |
| GLW7/OsSPL13 | Os07g0505200 | Transcription factor, target of miR156 | + | None | + | + | Expansion | Si et al, |
| OsmiR396e | Os04g0674500 | miRNA396 | − | − | − | − | Elongation and expansion | Miao et al, |
| OsmiR396f | Os02g0829000 | miRNA396 | − | − | − | − | Elongation and expansion | Miao et al, |
| SPL4 | Os02g0829000 | Target of miR156 | − | − | + | − | Elongation and division | Hu et al, |
| OsmiR167a | miRNA167 | + | / | / | + | Elongation | Qiao et al, | |
| OsmiR529a | miRNA529 | + | − | / | − | / | Yan et al, | |
| OsmiR408 | miRNA408 | + | + | / | + | Elongation | Yang et al, | |
Fig. 3. MicroRNAs control rice grain shape by targeting key transcription factor-encoding genes. MicroRNA156 (miR156) targets and down-regulates the genes encoding transcription factors OsSPL4, GW8/OsSPL16 and GLW7/OsSPL13. GLW7/OsSPL13 promotes the gene expression of SRS5. miR167a targets and inhibits OsARF6, which encodes an upstream transcription factor promoting the expression of OsAUX3 in the auxin signaling pathway. miR396 directs OsGRF4/GL2/GS2 and OsGRF8 mRNA silencing. OsGRF4/GL2/GS2 is an important cross-connect node of brassinosteroid (BR) signaling and miRNA regulatory pathway to determine the grain shape. OsGRF8 directly binds to the OsmiR408 promoter and may promote the accumulation of OsmiR408. Moreover, miR529a is involved in the grain shape determination by directing other OsSPL family genes. Regular arrows indicate positive regulation, while block arrows indicate negative regulation.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| brd1/OsBR6ox/ OsDWARF | Os03g0602300 | BR-6-oxidase | + | + | + | + | / | Mori et al, |
| D2 | Os01g0197100 | Cytochrome P450 CYP90D2 | + | + | + | + | / | Hong et al, |
| D11 | Os04g0469800 | Cytochrome P450 CYP724B1 | + | + | + | + | / | Tanabe et al, |
| OsBRI1/D61 | Os01g0718300 | BR receptor | + | + | None | + | / | Morinaka et al, |
| GW5/GSE5 | Os05g0187500 | Calmodulin binding protein | − | − | − | − | Proliferation | Wan et al, |
| GS5 | Os05g0158500 | Putative serine carboxypeptidase | None | + | / | + | Division and expansion | Li et al, |
| GL3.1/OsPPKL1 | Os03g0646900 | Phosphatase kelch (PPKL) family-Ser/Thr phosphatase | + | + | + | + | Proliferation | Hu et al, |
| GL2/GS2/ OsGRF4/GLW2 | Os02g0701300 | Transcription factor | − | − | + | − | Division and expansion | Che et al, |
| SLG | Os08g0562500 | BAHD aceltransferase-like protein | + | - | / | + | Elongation | Feng et al, |
| GS9 | Os09g0448500 | Transcription factor | − | + | None | None | Proliferation | Zhao et al, |
Table 5. Main regulators in brassinosteroid (BR) biosynthesis and signaling pathways for rice grain shape.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| brd1/OsBR6ox/ OsDWARF | Os03g0602300 | BR-6-oxidase | + | + | + | + | / | Mori et al, |
| D2 | Os01g0197100 | Cytochrome P450 CYP90D2 | + | + | + | + | / | Hong et al, |
| D11 | Os04g0469800 | Cytochrome P450 CYP724B1 | + | + | + | + | / | Tanabe et al, |
| OsBRI1/D61 | Os01g0718300 | BR receptor | + | + | None | + | / | Morinaka et al, |
| GW5/GSE5 | Os05g0187500 | Calmodulin binding protein | − | − | − | − | Proliferation | Wan et al, |
| GS5 | Os05g0158500 | Putative serine carboxypeptidase | None | + | / | + | Division and expansion | Li et al, |
| GL3.1/OsPPKL1 | Os03g0646900 | Phosphatase kelch (PPKL) family-Ser/Thr phosphatase | + | + | + | + | Proliferation | Hu et al, |
| GL2/GS2/ OsGRF4/GLW2 | Os02g0701300 | Transcription factor | − | − | + | − | Division and expansion | Che et al, |
| SLG | Os08g0562500 | BAHD aceltransferase-like protein | + | - | / | + | Elongation | Feng et al, |
| GS9 | Os09g0448500 | Transcription factor | − | + | None | None | Proliferation | Zhao et al, |
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| TGW6 | Os06g0623700 | Protein with IAA-glucose hydrolase activity | − | None | None | − | Proliferation and elongation | Ishimaru et al, |
| OsARF4 | Os01g0927600 | Transcription factor in auxin signaling | − | − | None | − | Expansion | Hu et al, |
| OsSK41/OsGSK5/GL3.3 | Os03g0841800 | GSK-like family member | − | − | / | − | Proliferation and elongation | Hu et al, et al, 2018 |
| qGL5/OsAUX3 | Os05g0447200 | Target genes in auxin signaling | − | None | / | − | Expansion | Qiao et al, |
Table 6. Main regulators in auxin biosynthesis and signaling pathway for rice grain shape.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| TGW6 | Os06g0623700 | Protein with IAA-glucose hydrolase activity | − | None | None | − | Proliferation and elongation | Ishimaru et al, |
| OsARF4 | Os01g0927600 | Transcription factor in auxin signaling | − | − | None | − | Expansion | Hu et al, |
| OsSK41/OsGSK5/GL3.3 | Os03g0841800 | GSK-like family member | − | − | / | − | Proliferation and elongation | Hu et al, et al, 2018 |
| qGL5/OsAUX3 | Os05g0447200 | Target genes in auxin signaling | − | None | / | − | Expansion | Qiao et al, |
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| OsCKX4 | Os01g0940000 | Cytokinin oxidase/dehydrogenase | − | − | / | − | Division | Gao et al, |
| OsVQ13 | Os03g0100020 | JA responsive protein | + | + | / | / | / | Uji et al, |
| BG3/OsPUP4 | Os01g0680200 | Purine permease 4 | + | + | + | + | Division | Xiao et al, |
| OsPUP7 | Os05g0556800 | Purine permease 4 | + | + | / | + | Division | Xiao et al, |
| GW6 | Os06g0266800 | GA-regulated GAST family protein | + | + | / | + | Expansion | Shi et al, |
| OsPUP1 | Os03g0187800 | Purine permease 1 | None | − | / | - | Division | Xiao et al, |
| AGO2 | Os04g0615700 | ARGONAUTE protein | + | None | / | + | Division | Yin et al, |
Table 7. Other plant hormones regulation for rice grain shape.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| OsCKX4 | Os01g0940000 | Cytokinin oxidase/dehydrogenase | − | − | / | − | Division | Gao et al, |
| OsVQ13 | Os03g0100020 | JA responsive protein | + | + | / | / | / | Uji et al, |
| BG3/OsPUP4 | Os01g0680200 | Purine permease 4 | + | + | + | + | Division | Xiao et al, |
| OsPUP7 | Os05g0556800 | Purine permease 4 | + | + | / | + | Division | Xiao et al, |
| GW6 | Os06g0266800 | GA-regulated GAST family protein | + | + | / | + | Expansion | Shi et al, |
| OsPUP1 | Os03g0187800 | Purine permease 1 | None | − | / | - | Division | Xiao et al, |
| AGO2 | Os04g0615700 | ARGONAUTE protein | + | None | / | + | Division | Yin et al, |
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| OsGIF1 | Os11g0615200 | Transcript co-activator | + | / | / | + | Proliferation | Duan et al, |
| OsGIF2 | Os12g0496900 | Transcript co-activator | + | / | / | + | Proliferation | Duan et al, |
| GW7/GL7/SLG7 | Os07g0603300 | TONNEAU1-recruiting motif protein | + | − | + | + | Proliferation | Wang S K et al, |
| OsFD2 | Os06g0720900 | bZIP transcription factor | − | − | − | − | Expansion and division | He et al, |
Table 8. Main regulators in other transcriptional regulatory pathway for rice grain shape.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| OsGIF1 | Os11g0615200 | Transcript co-activator | + | / | / | + | Proliferation | Duan et al, |
| OsGIF2 | Os12g0496900 | Transcript co-activator | + | / | / | + | Proliferation | Duan et al, |
| GW7/GL7/SLG7 | Os07g0603300 | TONNEAU1-recruiting motif protein | + | − | + | + | Proliferation | Wang S K et al, |
| OsFD2 | Os06g0720900 | bZIP transcription factor | − | − | − | − | Expansion and division | He et al, |
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| Cyclin-T1;3 | Os11g0157100 | Cell cycle regulator | + | / | / | / | Proliferation | Qi et al, |
| FUWA | Os02g0234200 | NHL domain-containing protein | + | − | + | − | Division | Chen et al, |
| GW6a/OsglHAT1 | Os06g0650300 | Histone H4 acetyltransferase | / | / | / | + | / | Song et al, |
| GF14f | Os03g0710800 | 14-3-3 protein | − | None | None | − | Expansion and division | Zhang et al, |
| MIS2/OsCR4 | Os03g0637800 | Receptor-like kinase | + | + | + | + | Expansion and division | Chun et al, |
| qTGW12a | Os12g0552600 | MATE transporter | / | + | / | + | / | Du et al, |
| OsDDM1b | Os03g0722400 | Subunit of chromatin remoeling complexes | + | + | / | / | Proliferation | Guo et al, |
| OsCEN2 | Os11g0152500 | CENTRORADIALIS family member | − | − | − | − | Expansion | He et al, |
| SMG3 | Os03g0410000 | MYB-like protein | − | − | / | − | Elongation and proliferation | Li et al, |
| qGSN5 | Os05g054860 | P-type PPR protein | + | + | / | + | Proliferation | Yuan et al, |
| SDR7-6 | Os07g0663900 | Short-chain alcohol dehydrogenase/reductase | None | + | + | None | / | Zheng et al, |
Table 9. Other regulators in rice grain shape determination.
| Gene | ID | Protein category | Regulatory role | Effect on cell | Reference | |||
|---|---|---|---|---|---|---|---|---|
| Length | Width | Thickness | Weight | |||||
| Cyclin-T1;3 | Os11g0157100 | Cell cycle regulator | + | / | / | / | Proliferation | Qi et al, |
| FUWA | Os02g0234200 | NHL domain-containing protein | + | − | + | − | Division | Chen et al, |
| GW6a/OsglHAT1 | Os06g0650300 | Histone H4 acetyltransferase | / | / | / | + | / | Song et al, |
| GF14f | Os03g0710800 | 14-3-3 protein | − | None | None | − | Expansion and division | Zhang et al, |
| MIS2/OsCR4 | Os03g0637800 | Receptor-like kinase | + | + | + | + | Expansion and division | Chun et al, |
| qTGW12a | Os12g0552600 | MATE transporter | / | + | / | + | / | Du et al, |
| OsDDM1b | Os03g0722400 | Subunit of chromatin remoeling complexes | + | + | / | / | Proliferation | Guo et al, |
| OsCEN2 | Os11g0152500 | CENTRORADIALIS family member | − | − | − | − | Expansion | He et al, |
| SMG3 | Os03g0410000 | MYB-like protein | − | − | / | − | Elongation and proliferation | Li et al, |
| qGSN5 | Os05g054860 | P-type PPR protein | + | + | / | + | Proliferation | Yuan et al, |
| SDR7-6 | Os07g0663900 | Short-chain alcohol dehydrogenase/reductase | None | + | + | None | / | Zheng et al, |
Fig. 4. Main genes regulating three-dimension of grain shape and their potential value in mechanized production of hybrid seeds. Genes with regulatory roles in the formation of grain length, grain width and grain thickness are highlighted in green, orange and purple, respectively. Red arrows indicate positive regulation, and blue block arrows indicate negative regulation. Red rectangles frame the genes with positive roles while blue rectangles frame genes with negative roles. The cylinder sorting, sieve sorting, gravity sorting systems can be used to separate hybrid rice seeds in dependence of grain length, grain thickness, and grain weight differences, respectively.
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