The homeotic gene long sterile lemma ( G1 ) specifies sterile lemma identity in the rice spikelet
Open accessAbstract
The mechanism of floral organ specification is principally conserved in angiosperms, as demonstrated by the ABC model. By contrast, mechanisms that regulate the development of organs or structures specific to a group of species remain unclear. Grasses have unique inflorescence units, comprising spikelets and florets. In the genus Oryza (rice), the single spikelet consists of a fertile floret subtended by a lemma and a palea, two sterile lemmas, and rudimentary glumes. Each sterile lemma is a tiny glume-like organ with a smooth surface. Here, we have examined a long sterile lemma1 ( g1 ) mutant, in which the sterile lemma is enlarged like the lemma. Detailed phenotypic analysis reveals that the large sterile lemma in the g1 mutant appears to be caused by homeotic transformation of the sterile lemma into a lemma, suggesting that G1 is involved in the repression of lemma identity to specify the sterile lemma. Gene isolation reveals that G1 is a member of a plant-specific gene family that encodes proteins with a previously uncharacterized domain, named here ALOG ( Arabidopsis LSH1 and Oryza G1 ). G1 mRNA is expressed in sterile lemma primordia throughout their development, and G1 protein is localized in the nucleus. A trans-activation assay using the yeast GAL4 system suggests that G1 is involved in transcriptional regulation. Repression of lemma identity by G1 is consistent with a hypothesis proposed to explain the morphological evolution of rice spikelets. We also show that a wild rice species, Oryza grandiglumis , that forms large sterile lemmas has serious mutations in the G1 gene.
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G1 in rice is homologous to Arabidopsis LSH3/4.
“| LSH3/4 | G1 (rice) | ALOG | Only gain-of-function | SAM and lateral organs | Takeda et al. (2011); Cho & Zam- |”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Yoshida et al. (2009)
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“To underscore the high conservation of the OBO domain, we also examined the amino acid sequence of a homolog, G1L1 (25), from the fern Selaginella moellendorffi.”
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BackgroundA conserved regulatory mechanism mediates the convergent evolution of plant shoot lateral organs
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“The G1/ELE gene only contains one exon and encodes one DUF640 domain protein which is localized to the nucleus (Yoshida et al., 2009; Hong et al., 2010).”
InfluentialHuang, X., Xiao, N., Zou, Y.-P., et al. (2022) · Genome biology · doi:10.1186/s13059-022-02646-6 · Cited by 44 · see citing works
Multifloret spikelet improves rice yield
Ren, D., Li, Y., He, G., & Qian, Q. (2019) · New Phytologist · doi:10.1111/nph.16303 · Cited by 44 · see citing works
Hirano, H., Tanaka, W., & Toriba, T. (2013) · Methods in molecular biology · doi:10.1007/978-1-4614-9408-9_3 · Cited by 42 · see citing works
Self-citationBELL 1 ‐like homeobox genes regulate inflorescence architecture and meristem maintenance in rice
Ikeda, T., Tanaka, W., Toriba, T., et al. (2019) · The Plant Journal · doi:10.1111/tpj.14230 · Cited by 39 · see citing works
“The 13-kb fragment was transferred into a pBI-Hm12-GW plasmid containing the Gateway rfC cassette (Invitrogen) (Yoshida et al., 2009).”
MethodSelf-citationEctopic expression of OsMADS1 caused dwarfism and spikelet alteration in rice
Wang, L., Zeng, X., Zhuang, H., et al. (2016) · Plant Growth Regulation · doi:10.1007/s10725-016-0220-9 · Cited by 38 · see citing works
Peng, P., Liu, L., Fang, J., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-14146-w · Cited by 38 · see citing works
Zhang, Y., Yu, H., Liu, J., et al. (2016) · Molecular Breeding · doi:10.1007/s11032-016-0578-4 · Cited by 35 · see citing works
“the floret contains a pair of interlocked lemma and palea, two lodicules, six stamens and a pistil (Yoshida et al. 2009).”
BackgroundMolecular and genetic pathways for optimizing spikelet development and grain yield
Yuan, Z., Persson, S., & Zhang, D. (2020) · aBIOTECH · doi:10.1007/s42994-020-00026-x · Cited by 37 · see citing works
Regulation of meristem maintenance and organ identity during rice reproductive development
Chongloi, G. L., Prakash, S., & Vijayraghavan, U. (2019) · Journal of Experimental Botany · doi:10.1093/jxb/erz046 · Cited by 33 · see citing works
MORE FLORET1 Encodes a MYB Transcription Factor That Regulates Spikelet Development in Rice
Ren, D., Rao, Y., Yu, H., et al. (2020) · PLANT PHYSIOLOGY · doi:10.1104/pp.20.00658 · Cited by 34 · see citing works
“Previous studies showed that OsMADS34, ASP1, EG1, FON4, and G1 function in the development of the sterile lemma (Li et al., 2009; Yoshida et al., 2009, 2012; Gao et al., 2010; Hong et al., 2010; Lin et al., 2014).”
BackgroundThe C2H2 zinc-finger protein LACKING RUDIMENTARY GLUME 1 regulates spikelet development in rice
Xu, Q., Yu, H., Xia, S., et al. (2020) · 中国科学通报：英文版 · doi:10.1016/j.scib.2020.01.019 · Cited by 32 · see citing works
“Similarly, in the pap2/osmads34 and asp1 (aberrant spikelet and panicle 1) mutants, the rudimentary glumes and sterile lemmas were elongated and exhibited a lemma-like identity [10–12,49], and in the g1, eg1, and fon4 mutants, the sterile lemmas were homeotically transformed into lemmas [9,13,19].”
BackgroundInfluentialTanaka, W., & Hirano, H. (2019) · New Phytologist · doi:10.1111/nph.16163 · Cited by 31 · see citing works
“After digestion of the pTAB1-WOX4-pBluescript construct with BamH1, the fragments were inserted into a pENTR 2B vector (Invitrogen) and then transferred into a pBI-Hm12-GW vector containing the Gateway rfC cassette (Invitrogen) by LR recombination (Yoshida et al., 2009).”
MethodSelf-citationRegulatory Role of OsMADS34 in the Determination of Glumes Fate, Grain Yield, and Quality in Rice
Ren, D., Rao, Y., Leng, Y., et al. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.01853 · Cited by 30 · see citing works
“Meantime, G1and ASP1 were maily expressed in rudimentary glumes and/or sterile lemmas, and restrained the elongation of glumes (Yoshida et al., 2009, 2012).”
BackgroundMethodInfluentialRieu, P., Beretta, V. M., Caselli, F., Thévenon, E., Lucas, J., Rizk, M., Franchini, E., Caporali, E., Paleni, C., Nanao, M., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2310464121 · Cited by 29 · see citing works
Naramoto, S., Hata, Y., & Kyozuka, J. (2020) · Journal of Plant Research · doi:10.1007/s10265-020-01171-6 · Cited by 29 · see citing works
Repurposing of Anthocyanin Biosynthesis for Plant Transformation and Genome Editing
He, Y., Zhu, M., Wu, J., et al. (2020) · Frontiers in Genome Editing · doi:10.3389/fgeed.2020.607982 · Cited by 27 · see citing works
“When G1 is disrupted, the length of the sterile lemma increased dramatically, providing an easily scorable phenotype (Yoshida et al., 2009).”
BackgroundThe ALOG family members OsG1L1 and OsG1L2 regulate inflorescence branching in rice
Beretta, V. M., Franchini, E., Din, I. U., et al. (2023) · The Plant Journal · doi:10.1111/tpj.16229 · Cited by 27 · see citing works
Tanaka, W., Toriba, T., & Hirano, H. (2014) · Advances in botanical research · doi:10.1016/b978-0-12-417162-6.00008-0 · Cited by 26 · see citing works
Self-citationYoo, J.-H., Park, J.-H., Cho, S., et al. (2011) · Plant Molecular Biology · doi:10.1007/s11103-011-9839-0 · Cited by 26 · see citing works
BEAK LIKE SPIKELET1 is Required for Lateral Development of Lemma and Palea in Rice
Ma, X., Cheng, Z., Wu, F., et al. (2012) · Plant Molecular Biology Reporter · doi:10.1007/s11105-012-0480-0 · Cited by 25 · see citing works
Meng, Q., Li, X., Zhu, W., Yang, L. C., Liang, W., Dreni, L., & Zhang, D. (2017) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12594 · Cited by 24 · see citing works
Zhang, D., Yuan, Z., An, G., Dreni, L., Hu, J., & Kater, M. M. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7903-1_19 · Cited by 23 · see citing works
Takanashi, H., Kajiya‐Kanegae, H., Nishimura, A., Yamada, J., Ishimori, M., Kobayashi, M., Yano, K., Iwata, H., Tsutsumi, N., & Sakamoto, W. (2022) · Plant and Cell Physiology · doi:10.1093/pcp/pcac057 · Cited by 23 · see citing works
A role for TRIANGULAR HULL1 in fine-tuning spikelet morphogenesis in rice
Sato, D.-S., Ohmori, Y., Nagashima, H., et al. (2014) · Genes & Genetic Systems · doi:10.1266/ggs.89.61 · Cited by 23 · see citing works
Self-citationHe, L., Lei, Y., Li, X., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21114060 · Cited by 20 · see citing works
“In rice, the ALOG family gene G1 regulates the growth of the sterile lemma in the spikelet [8].”
BackgroundThe Birth and Death of Floral Organs in Cereal Crops
Huang, Y., & Schnurbusch, T. (2024) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-060223-041716 · Cited by 20 · see citing works
Zhu, C., Yang, J., Box, M. S., Kellogg, E. A., & Eveland, A. L. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.01309 · Cited by 20 · see citing works
“Functional studies of other ALOG genes in various species indicate that they generally share a role in developmental phase changes and organ identity, and their spatiotemporal expression patterns determine their specificity (Yoshida et al., 2009; Cho and Zambryski, 2011; Takeda et al., 2011).”
BackgroundGenome-Wide Identification and Characterization of the ALOG Domain Genes in Rice
Li, N., Wang, Y., Lu, J. N., et al. (2019) · International Journal of Genomics · doi:10.1155/2019/2146391 · Cited by 20 · see citing works
Phan, M. S. V., Keren, I., Tran, P. T., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-04424-x · Cited by 19 · see citing works
Huang, X., Tang, L., Yu, Y., et al. (2018) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2018.03.008 · Cited by 19 · see citing works
A member of the ALOG gene family has a novel role in regulating nodulation in Lotus japonicus
Lei, Y., Su, S., He, L., et al. (2018) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12711 · Cited by 19 · see citing works
Dong, K., Wu, F., Cheng, S., et al. (2024) · Molecular Plant · doi:10.1016/j.molp.2024.04.014 · Cited by 18 · see citing works
Zhou, S., Yan, B., Li, F., et al. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01644 · Cited by 18 · see citing works
“SNP-17 BAI52979 G1-like1 protein Floral organs development (Yoshida et al., 2009)”
BackgroundDong, X., Lee, J., Nou, I., & Hur, Y. (2014) · Plant Breeding and Biotechnology · doi:10.9787/pbb.2014.2.2.126 · Cited by 17 · see citing works
“Rice LONG STERILE LEMMA (G1), the first identified ALOG gene from monocots, specifies the identity of the sterile lemma by repressing lemma identity via the regulation of downstream target genes (Yoshida et al. 2009).”
BackgroundMolecular characterization of Arabidopsis thaliana LSH1 and LSH2 genes
Lee, M., Dong, X., Song, H., Yang, J. Y., Kim, S., & Hur, Y. (2020) · Genes & Genomics · doi:10.1007/s13258-020-00985-x · Cited by 17 · see citing works
Zou, J., Li, Z., Tang, H., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910314 · Cited by 17 · see citing works
“All members of the LSH family have a highly conserved Domain of Unknown Function 640 (DUF640) domain, which is also called the Arabidopsis LSH1 and Oryza G1 (ALOG) domain in the Pfam protein database [22,23].”
BackgroundWang, Y., Bi, X., & Zhong, J. (2022) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiac257 · Cited by 17 · see citing works
OsBBX19-OsBTB97/OsBBX11 module regulates spikelet development and yield production in rice
Shalmani, A., Ullah, U., Li, T., Zhang, R., Jing, X., Muhammad, I., Bhanbhro, N., Liu, W., Li, W., & Chen, K. (2023) · Plant Science · doi:10.1016/j.plantsci.2023.111779 · Cited by 17 · see citing works
Xiao, W., Ye, Z., Yao, X., et al. (2018) · BMC Plant Biology · doi:10.1186/s12870-018-1431-1 · Cited by 17 · see citing works
Genome-wide identification and characterization of the ALOG gene family in Petunia
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“family (Pfam) database (Pfam accession number IPR006936) was identified in ALOG family [4, 5].”
BackgroundInfluentialThe RNA binding protein OsLa influences grain and anther development in rice
Guo, H., Cui, Y., Huang, L., et al. (2022) · The Plant Journal · doi:10.1111/tpj.15746 · Cited by 15 · see citing works
Lin, Y., Laosatit, K., Chen, J., et al. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.575922 · Cited by 15 · see citing works
“DUF640 is a transcription factor that regulates the late development of lemma and palea in rice (Yoshida et al., 2009; Ma et al., 2013).”
BackgroundKnown types of membrane-less organelles and biomolecular condensates
Darling, A. L., & Uversky, V. N. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-823967-4.00002-6 · Cited by 15 · see citing works
The ABC of Flower Development in Monocots: The Model of Rice Spikelet
Dreni, L. (2023) · Methods in molecular biology · doi:10.1007/978-1-0716-3299-4_3 · Cited by 14 · see citing works
Nan, W., Shi, S., Jeewani, D. C., et al. (2018) · Genes · doi:10.3390/genes9100510 · Cited by 14 · see citing works
“Different DUF families play various roles in stress responses and plant development [5,16,19,27,28].”
BackgroundHan, X., Wu, X., Zhang, Y., et al. (2025) · The Plant Cell · doi:10.1093/plcell/koaf062 · Cited by 13 · see citing works
How leaves of mycoheterotrophic plants evolved – from the view point of a developmental biologist
Tsukaya, H. (2018) · New Phytologist · doi:10.1111/nph.14994 · Cited by 13 · see citing works
“Another candidate gene is LONG STERILE LEMMA1 (G1) of rice (Yoshida et al., 2009).”
BackgroundWang, S., Chen, W., Xiao, W., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0133696 · Cited by 13 · see citing works
“Other genes that have been reported to be associated with rice hull development include frizzy panicle (FZP) [18], abnormal hull (ah) [19], sterile lemma (G1) [20], and elongated empty glume (ELE) [21].”
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A homolog of the ALOG family controls corolla tube differentiation in Torenia fournieri
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Cytokinin and ALOG proteins regulate pluripotent stem cell identity in the moss Physcomitrium patens
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A hybrid sterile locus leads to the linkage drag of interspecific hybrid progenies
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“2-cM region flanked by RM20943 and RM5752, and is adjacent to long sterile lemma (G1) (Yoshida et al., 2009; Liu et al., 2016).”
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OsVIL2 Regulates Spikelet Development by Controlling Regulatory Genes in Oryza sativa
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“Expression of REP1, DP1, and OsIG1 was reduced in osvil2 mutants, suggesting that those genes are linked with the palea defects.”
BackgroundInfluentialLv, Y., Zhang, X., Hu, Y., Liu, S., Yin, Y., & Wang, X. (2023) · Frontiers in Plant Science · doi:10.3389/fpls.2023.1162828 · Cited by 10 · see citing works
“The mfs1 mutant shows a delayed transition of spikelet meristems to floral meristems, resulting in an extra hull-like organ and an elongated rachilla (Yoshida et al., 2009; Ren et al., 2013).”
BackgroundLaFountain, A. M., Lin, Q., McMahon, H. E., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114444 · Cited by 10 · see citing works
Regulating Plant Architecture to Enhance the Future of Cereal Crop Production
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“Genes like SNB , OsIDS1 , and LSL are critical for spikelet development and meristem identity, influencing branching and spikelet formation (Lee and An 2012; Ren et al. 2013; Yoshida et al. 2009).”
- Authors
- Yoshida, A., Suzaki, T., Tanaka, W., & Hirano, H.-Y.
- Affiliations
- The University of Tokyo (JP)
- University of California San Diego (US)
- Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-8654, Japan
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-11-24
- Volume
- 106
- Issue
- 47
- Pages
- 20103-20108
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2775035
- OpenAlex
- W2032677611
- Semantic Scholar
- 82ab49c65d5a71c52986815cb49faa36656b9119
- Cited by
- 194
- References
- 47
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 33 · 2023: 18 · 2022: 13 · 2021: 7 · 2020: 15 · 2019: 20 · 2018: 10 · 2017: 9 · 2016: 9 · 2015: 6 · 2014: 10 · 2013: 9 · 2012: 7
- FWCI
- 6.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology
- Japan Science Society
- Japan Society for the Promotion of Science (20061006, 20380005)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Genetic and Mutation Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
- Keywords
- homeotic transformation, transcriptional regulation, Oryza grandiglumis, floral organ specification, rice
- MeSH terms
- Genes, Homeobox, Mutation, Phenotype, Phylogeny, Plant Proteins, Oryza, Genes, Plant, Gene Expression Regulation, Plant, Flowers
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