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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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“| LSH3/4 | G1 (rice) | ALOG | Only gain-of-function | SAM and lateral organs | Takeda et al. (2011); Cho & Zam- |”
From Divide et impera: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Yoshida et al. (2009)
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BackgroundSelf-citationLiu, H., Guo, S., Xu, Y., Li, C., Zhang, Z., Zhang, D., Xu, S., Zhang, C., & Chong, K. (2014) · PLANT PHYSIOLOGY · doi:10.1104/pp.114.235564 · Cited by 245
“Multiple genes, including G1 (Elongated Empty Glume) and OsMADS34, are required for lemma identity (Yoshida et al., 2009; Gao et al., 2010; Hong et al., 2010), and mutation of key floral regulator genes disrupts the morphology of the palea and lemma, for instance, in the leafy hull sterile1/osmads1…”
BackgroundMolecular Control of Grass Inflorescence Development
Zhang, D., & Yuan, Z. (2014) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050213-040104 · Cited by 233
“G1/ELE defines spikelet morphology by specifying sterile lemma identity, and g1/ele mutants exhibit a homeotic conversion of sterile lemma to lemma-like structures (53, 155).”
BackgroundThe SEPALLATA-Like Gene OsMADS34 Is Required for Rice Inflorescence and Spikelet Development
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“The G1/ELE expression is detectable in sterile lemma primordia throughout their development, suggesting that G1/ELE is key regulator for repressing lemma identity at the sterile lemma positions during rice spikelet development (Yoshida et al., 2009; Hong et al., 2010).”
BackgroundA genetic playground for enhancing grain number in cereals
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“After digestion with BamHI, the fragments were inserted into a pENTR 2B vector (Invitrogen) and then transferred into a pBI-Hm12-GW vector, which contains the Gateway rfC cassette (Invitrogen), by LR recombination (Yoshida et al., 2009).”
MethodSelf-citationRice Functional Genomics Research: Past Decade and Future
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“organ of the SM between the fertile floret and the rudimentary glume (Yoshida et al. 2009).”
BackgroundSelf-citationDreni, L., Pilatone, A., Yun, D., Erreni, S., Pajoro, A., Caporali, E., Zhang, D., & Kater, M. M. (2011) · The Plant Cell · doi:10.1105/tpc.111.087007 · Cited by 170
“Using in situ hybridization experiments, we also investigated the expression of G1/ELE, which is a specific marker for the sterile lemmas and palea that is not expressed in the lemma (Yoshida et al., 2009; Hong et al., 2010).”
BackgroundControl of inflorescence architecture in tomato by BTB/POZ transcriptional regulatorsPreprint
Cao, X., Park, S. J., Eck, J. M. V., & Lippman, Z. B. (2016) · Genes & Development · doi:10.1101/gad.288415.116 · Cited by 168
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“(D) and (H) In situ localization of LHS1 transcripts.”
BackgroundMethodInfluentialSelf-citationNew insights into the regulation of inflorescence architecture
Teo, Z. W. N., Song, S., Wang, Y., et al. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.11.001 · Cited by 148
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“In the g1/ele1mutant, sterile lemmas were found to be homeotically transformed into lemmas (Yoshida et al., 2009; Hong et al., 2010).”
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Self-citationTakeda, S., Hanano, K., Kariya, A., Shimizu, S., Zhao, L., Matsui, M., Tasaka, M., & Aida, M. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04571.x · Cited by 146
“Both LSH1 and G1 proteins localize to the nucleus, and G1 showed transactivation activity, indicating that ALOG proteins are involved in transcriptional regulation (Zhao et al., 2004; Yoshida et al., 2009).”
InfluentialLATERAL FLORET 1 induced the three-florets spikelet in rice
Zhang, T., Li, Y., Ma, L., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1700504114 · Cited by 135
Of floral fortune: tinkering with the grain yield potential of cereal crops
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Divide et impera: boundaries shape the plant body and initiate new meristems
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Distinct Regulation of Adaxial-Abaxial Polarity in Anther Patterning in Rice
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“The ta-siRNAs are then loaded into an RNA-induced silencing complex containing ARGONAUTE (AGO) protein and function in the cleavage of target mRNA (Allen et al., 2005; Xie et al., 2005; Yoshikawa et al., 2005).”
BackgroundInfluentialSelf-citationFZP determines grain size and sterile lemma fate in rice
Ren, D., Hu, J., Xu, Q., et al. (2018) · Journal of Experimental Botany · doi:10.1093/jxb/ery264 · Cited by 85
“The sterile lemma was regarded as the remnant of the morphologically modified lemma (Yoshida et al., 2009).”
InfluentialDebernardi, J. M., Greenwood, J. R., Finnegan, E. J., et al. (2019) · The Plant Journal · doi:10.1111/tpj.14528 · Cited by 79
“By contrast, rice mutants have been identified that affect the glume–lemma transition (Prasad et al., 2001; Yoshida et al., 2009, 2012; Gao et al., 2010; Hong et al., 2010; Lin et al., 2014; Wang et al., 2017; Wu et al., 2018) and the differentiation of the axillary meristem (Zhang et al., 2017)…”
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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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Os PEX 5 regulates rice spikelet development through modulating jasmonic acid biosynthesis
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“…STERILE LEMMA1 (G1), MULTI-FLORETS SPIKELET 1 (MFS1), LATERAL FLORET 1 (LF1) and many MADS-box genes including OsMADS1, OsMADS7 and OsMADS14 (Lim et al., 2000; Komatsu et al., 2003; Lee et al., 2007; Yoshida et al., 2009; Cui et al., 2010; Lee & An, 2012; Ren et al., 2013; Zhang et al., 2017).”
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“Recently, several mutants and their underlying genes related to the development of glume-like organs have been identified in rice, including eg1 (Li et al., 2009), long sterile lemma (g1; Yoshida et al., 2009)/elongated empty glume1 (ele1; Hong et al., 2010) and osmads34 (Gao et al., 2010).”
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Self-citationInterpreting lemma and palea homologies: a point of view from rice floral mutants
Lombardo, F., & Yoshida, H. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00061 · Cited by 61
“The g1 mutant shows the striking phenotype of sterile lemmas transformed into lemmas, bringing genetic evidence to the long-standing hypothesis by Arber (1934; Yoshida et al., 2009).”
BackgroundFON 4 prevents the multi‐floret spikelet in rice
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“Previous studies have shown that the mutation of G1, DF1/EG1 or OsMADS34 caused the formation of lemma-like sterile lemmas, whereas the mutation of LF1 induced the formation of lateral florets without lemmas (Li et al., 2009; Lin et al., 2014; Yoshida et al., 2009; Zhang et al., 2017).”
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“Specific transcription factors (TFs) bind DNA sequences distinct from the promoter elements recognized by the basal TFs to activate or repress transcription [1].”
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“Ultimately, the candidate mutations were experimentally validated using phenotype association assay.”
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“Mutations in G1/LONG SLENDER LEMMA1 (Yoshida et al., 2009; Yang et al., 2020) shift the size and cellular morphology of the sterile lemmas to look more like true lemmas, whereas mutations in other genes lead to stronger similarity between the sterile lemmas and rudimentary (true) glumes (summarized by Ren et al., 2018…”
BackgroundA conserved regulatory mechanism mediates the convergent evolution of plant shoot lateral organs
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“ALOG proteins may mediate diversification of lateral organs during plant evolution It has been suggested that the repressive activity of the OsG1 gene on growth led to the evolution of the rice spikelet [29].”
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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).”
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Multifloret spikelet improves rice yield
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“The 13-kb fragment was transferred into a pBI-Hm12-GW plasmid containing the Gateway rfC cassette (Invitrogen) (Yoshida et al., 2009).”
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“the floret contains a pair of interlocked lemma and palea, two lodicules, six stamens and a pistil (Yoshida et al. 2009).”
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“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).”
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“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].”
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“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).”
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“Meantime, G1and ASP1 were maily expressed in rudimentary glumes and/or sterile lemmas, and restrained the elongation of glumes (Yoshida et al., 2009, 2012).”
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“When G1 is disrupted, the length of the sterile lemma increased dramatically, providing an easily scorable phenotype (Yoshida et al., 2009).”
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Beretta, V. M., Franchini, E., Din, I. U., et al. (2023) · The Plant Journal · doi:10.1111/tpj.16229 · Cited by 27
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BEAK LIKE SPIKELET1 is Required for Lateral Development of Lemma and Palea in Rice
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“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
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“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
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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
Dong, K., Wu, F., Cheng, S., Li, S., Zhang, F., Xing, X., Jin, X., Luo, S., Feng, M., Miao, R., et al. (2024) · Molecular Plant · doi:10.1016/j.molp.2024.04.014 · Cited by 19
Zhou, S., Yan, B., Li, F., et al. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01644 · Cited by 18
“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
“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
Zou, J., Li, Z., Tang, H., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910314 · Cited by 17
“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
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
Xiao, W., Ye, Z., Yao, X., He, L., Lei, Y., Luo, D., & Su, S. (2018) · BMC Plant Biology · doi:10.1186/s12870-018-1431-1 · Cited by 17
Genome-wide identification and characterization of the ALOG gene family in Petunia
Chen, F., Zhou, Q., Wu, L., et al. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-2127-x · Cited by 17
“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
Lin, Y., Laosatit, K., Chen, J., et al. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.575922 · Cited by 15
“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
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
Nan, W., Shi, S., Jeewani, D. C., et al. (2018) · Genes · doi:10.3390/genes9100510 · Cited by 14
“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
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
“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
“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].”
BackgroundZhou, B., Zhou, Z., Ding, J., et al. (2018) · The Plant Genome · doi:10.3835/plantgenome2017.11.0107 · Cited by 13
A homolog of the ALOG family controls corolla tube differentiation in Torenia fournieri
Xiao, W., Su, S., Higashiyama, T., et al. (2019) · Development · doi:10.1242/dev.177410 · Cited by 13
Cytokinin and ALOG proteins regulate pluripotent stem cell identity in the moss Physcomitrium patens
Hata, Y., Ohtsuka, J., Hiwatashi, Y., et al. (2024) · Science Advances · doi:10.1126/sciadv.adq6082 · Cited by 12
A hybrid sterile locus leads to the linkage drag of interspecific hybrid progenies
Wang, M., Yang, J., Wan, J., et al. (2020) · Acta Botanica Yunnanica · doi:10.1016/j.pld.2020.07.003 · Cited by 12
“2-cM region flanked by RM20943 and RM5752, and is adjacent to long sterile lemma (G1) (Yoshida et al., 2009; Liu et al., 2016).”
BackgroundLiu, K., Li, M., Zhang, B., et al. (2022) · Rice Science · doi:10.1016/j.rsci.2021.11.001 · Cited by 12
OsVIL2 Regulates Spikelet Development by Controlling Regulatory Genes in Oryza sativa
Yoon, H., Yang, J., Liang, W., et al. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.00102 · Cited by 11
“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
“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., Min, Y., Ding, B., Gurung, V., Seemann, J. R., & Yuan, Y. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114444 · Cited by 8
Regulating Plant Architecture to Enhance the Future of Cereal Crop Production
Sandhu, N., Aggarwal, H., Kumar, A., et al. (2025) · Physiologia Plantarum · doi:10.1111/ppl.70367 · Cited by 9
“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).”
Metadata
- 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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