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Genetic characterization and linkage analysis of spotted leaf 6, liguleless and lax panicle traits in mutant rice

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Abstract

Phenotypic mutants are valuable resources for elucidating the function of genes responsible for their expression. This study examined mutant rice strains expressing three traits: spotted leaf 6 (spl6), lax panicle (lax), and liguleless (lg). In the mutant, the spl6 phenotype was a genetically programmed lesion-mimicking mutation (LMM) that displayed spontaneously scattered spots across the leaf surface. In the lg trait, the plant lacked a collar region, and there were no auricles and ligules at the junction of the leaf blade and leaf sheath. The lax panicle trait manifested as sparely arranged spikelets resulting from the terminal spikelet with no lateral spikelets, which caused a drastic reduction of the total seed number in the mutant. All three mutant genes were genetically recessive and had nuclear gene regulation. The dihybrid segregation of the lg gene was classified independently according to the Mendelian 9:3:3:1 dihybrid segregation ratio in the F2 generation, suggesting that the lg gene is not linked to the same chromosome as the lax and spl6 genes. On the other hand, spl6 and lax were not assorted independently, indicating that they are closely linked on chromosome 1 in rice. Additional linkage analysis from the recombination of spl6 and lax genes reconfirmed that the two genes were ~9.4 cM away from each other. The individual single-gene mutant plant from one plant with a three-gene mutation (spl6, lax, and lg) was isolated and characterized, which will be a crucial resource for the gene cloning and molecular characterization of these genes.

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Modified from Yoshimura et al. (1997).

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References

  • Balagué C., Lin B., Alcon C., Flottes G., Malmström S., Köhler C. et al. 2003 HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15, 365–379.

    Article  PubMed  PubMed Central  Google Scholar 

  • Becraft P. W., Bongard-Pierce D. K., Sylvester A. W., Poethig R. S. and Freeling M. 1990 The liguleless-1 gene acts tissue specifically in maize leaf development. Dev. Biol. 141, 220–232.

    Article  CAS  PubMed  Google Scholar 

  • Bell A. D., Bryan A. 2008 Plant form: an illustrated guide to flowering plant morphology. Oxford University Press, Oxford.

    Google Scholar 

  • Bruggeman Q., Raynaud C., Benhamed M. and Delarue M. 2015 To die or not to die? Lessons from lesion mimic mutants. Front. Plant Sci. 6, 24.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai L., Yan M., Yun H., Tan J., Du D., Sun H. et al. 2021 Identification and fine mapping of lesion mimic mutant spl36 in rice (Oryza sativa L.). Breed. Sci. 71, 510–519.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z., Yin W., Li X., Lu T., Ye H., Dai G. et al. 2022 OsSPL88 Encodes a cullin protein that regulates rice growth and development. Front. Genet. 13, 918973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai D., Chen J., Du C., Liang M., Wu M., Mou T. et al. 2022 A 2-MB chromosome inversion interrupted transcription of lax2-4 and generated pleiotropic phenotypes in rice. J. Plant Growth Regul. 41, 2328–2337.

    Article  CAS  Google Scholar 

  • Fowler J. E. and Freeling M. 1996 Genetic analysis of mutations that alter cell fates in maize leaves: dominant Liguleless mutations. Dev. Genet. 18, 198–222.

    Article  CAS  PubMed  Google Scholar 

  • Futsuhara Y., Kondo S., Kitano H. and Mii M. 1979 Genetical studies on dense and lax panicles in rice: I. Character expression and mode of lax panicle rice. Jpn. J. Breed. 29, 151–158.

    Article  Google Scholar 

  • Harper L. and Freeling M. 1996 Interactions of liguleless1 and liguleless2 function during ligule induction in maize. Genetics 144, 1871–1882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoshikawa K. 1989 The growing rice plant. An anatomical monograph, pp. 199–205. Nosan Gyoson Bunka kyokai, Tokyo.

  • Jiang R., Zhou S., Da X., Chen T., Xu J., Yan P. and Mo X. 2022 Ubiquitin-specific protease 2 (OsUBP2) negatively regulates cell death and disease resistance in rice. Plants 11, 2568.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang S. G., Matin M. N., Bae H. and Natarajan S. 2007 Proteome analysis and characterization of phenotypes of lesion mimic mutant spotted leaf 6 in rice. Proteomics 7, 2447–2458.

    Article  CAS  PubMed  Google Scholar 

  • Kang S. G., Lee K. E., Singh M., Kumar P. and Matin M. N. 2021 Rice lesion mimic mutants (LMM): The current understanding of genetic mutations in the failure of ROS scavenging during lesion formation. Plants 10, 1598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kinoshita T. 1995 Report of committee on gene symbolization, nomenclature and linkage groups. Rice Genet. Newslett. 12, 9–154.

    Google Scholar 

  • Kishimoto N., Shimosaka E., Matsuura S. and Saito A. 1992 A current RFLP linkage map of rice: Alignment of the molecular map with the classical map. Rice Genet. Newslett. 9, 118–124.

    Google Scholar 

  • Komatsu M., Maekawa M., Shimamoto K. and Kyozuka J. 2001 The LAX1 and FRIZZY PANICLE 2 genes determine the inflorescence architecture of rice by controlling rachis-branch and spikelet development. Dev. Biol. 231, 364–373.

    Article  CAS  PubMed  Google Scholar 

  • Komatsu M., Chujo A., Nagato Y., Shimamoto K. and Kyozuka J. 2003 FRIZZY PANICLE is required to prevent the formation of axillary meristems and to establish floral meristem identity in rice spikelets. Development 130, 3841–4385.

    Article  CAS  PubMed  Google Scholar 

  • Kumamaru T., Satoh H., Iwata N., Omura T., Ogawa M. and Tanaka K. 1988 Mutants for rice storage proteins: 1. Screening of mutants for rice storage proteins of protein bodies in the starchy endosperm. Theor. Appl. Genet. 76, 11–16.

    Article  CAS  PubMed  Google Scholar 

  • Lee D.-Y., Lee J., Moon S., Park S. Y. and An G. 2007a The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem. Plant J. 49, 64–78.

    Article  CAS  PubMed  Google Scholar 

  • Lee J., Park J.-J., Kim S. L., Yim J. and An G. 2007b Mutations in the rice liguleless gene result in a complete loss of the auricle, ligule, and laminar joint. Plant Mol. Biol. 65, 487–499.

    Article  CAS  PubMed  Google Scholar 

  • Li G., Zhang H., Li J., Zhang Z. and Li Z. 2021 Genetic control of panicle architecture in rice. Crop J. 9, 590–597.

    Article  Google Scholar 

  • Li C., Liu H., Wang J., Pan Q., Wang Y., Wu K. et al. 2022 Characterization and fine mapping of a lesion mimic mutant (Lm5) with enhanced stripe rust and powdery mildew resistance in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 135, 421–438.

    Article  CAS  PubMed  Google Scholar 

  • Liu G., Wang L., Zhou Z., Leung H., Wang G. L. and He C. 2004 Physical mapping of a rice lesion mimic gene, Spl1, to a 70-kb segment of rice chromosome 12. Mol. Genet. Genomics 272, 108–115.

    Article  CAS  PubMed  Google Scholar 

  • Liu K., Cao J., Yu K., Liu X., Gao Y., Chen Q. et al. 2019 Wheat TaSPL8 modulates leaf angle through auxin and brassinosteroid signaling. Plant Physiol. 181, 179–194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu R., Lu J., Zheng S., Du M., Zhang C., Wang M. et al. 2021 Molecular mapping of a novel lesion mimic gene (lm4) associated with enhanced resistance to stripe rust in bread wheat. BMC Genomic Data 22, 1–9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lv Y., Zhang X., Hu Y., Liu S., Yin Y. and Wang X. 2023 BOS1 is a basic helix–loop–helix transcription factor involved in regulating panicle development in rice. Front. Plant Sci. 14, 1162828.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma J., Wang Y., Ma X., Meng L., Jing R., Wang F. et al. 2019 Disruption of gene SPL 35, encoding a novel CUE domain-containing protein, leads to cell death and enhanced disease response in rice. Plant Biotechnol. J. 17, 1679–1693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maekawa M. 1988 A new allele at the lg locus conferring short ligule. Rice Genet. Newslett. 5, 87–89.

    Google Scholar 

  • Maekawa M., Kinoshita T. and Takahashi M. 1981 A new gametophyte gene in the second linkage group of rice: genetical studies on rice plant. LXXVI. J. Fac. Agric. Hokkaido Univ. 60, 107–114.

    Google Scholar 

  • Matin M. N. and Kang S. G. 2012 Genetic and phenotypic analysis of lax1-6, a mutant allele of LAX PANICLE1 in rice. J. Plant Biol. 55, 50–63.

    Article  CAS  Google Scholar 

  • Matin M. N., Suh H. S. and Kang S. G. 2006 Characterization of phenotypes of rice lesion resembling disease mutants. Korean J. Genet. 28, 221–228.

    CAS  Google Scholar 

  • McSteen P., Laudencia-Chingcuanco D. and Colasanti J. 2000 A floret by any other name: control of meristem identity in maize. Trend. Plant Sci. 5, 61–66.

    Article  CAS  Google Scholar 

  • Mori K., Kinoshita T. and Takahashi M. 1973 Linkage relationships of genes for some mutant characters of rice kept in Kyushu University-Genetical studies on rice plant. LV. Mem. Fac. Agr. Hokkaido Univ. 8, 377–385.

    Google Scholar 

  • Mori M., Tomita C., Sugimoto K., Hasegawa M., Hayashi N., Dubouzet J. G. et al. 2007 Isolation and molecular characterization of a Spotted leaf 18 mutant by modified activation-tagging in rice. Plant Mol. Biol. 63, 847–860.

    Article  CAS  PubMed  Google Scholar 

  • Morinaga T. 1938 Inheritance in rice, Oryza sativa L., II. Linkage between the gene for purple plant color and the gene for liguleless. Jpn. J. Bot. 9, 121–129.

    Google Scholar 

  • Muehlbauer G. J., Fowler J. E. and Freeling M. 1997 Sectors expressing the homeobox gene liguleless3 implicate a time-dependent mechanism for cell fate acquisition along the proximal-distal axis of the maize leaf. Development 124, 5097–5106.

    Article  CAS  PubMed  Google Scholar 

  • Nagao S. and Takahashi M. 1963 Trial Construction of Twelve Linkage Groups in Japanese Rice:(Genetical Studies on Rice Plant, XXVII). J. Fac. Agric. Hokkaido Univ. 53, 72–130.

    Google Scholar 

  • Nagato Y. and Yoshimura A. 1998 Report of the committee on gene symbolization, nomenclature and linkage map. Rice Genet. Newslett. 15, 13–74.

    Google Scholar 

  • Oikawa T. and Kyozuka J. 2009 Two-step regulation of LAX PANICLE1 protein accumulation in axillary meristem formation in rice. Plant Cell 21, 1095–1108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin L., Wu X. and Zhao H. 2023 Molecular and functional dissection of LIGULELESS1 (LG1) in plants. Front. Plant Sci. 14, 1190004.

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiu Z., Zhu L., He L., Chen D., Zeng D., Chen G. et al. 2019 DNA damage and reactive oxygen species cause cell death in the rice local lesions 1 mutant under high light and high temperature. New Phytol. 222, 349–365.

    Article  CAS  PubMed  Google Scholar 

  • Ruan B., Hua Z., Zhao J., Zhang B., Ren D., Liu C. et al. 2019 Os ACL-A2 negatively regulates cell death and disease resistance in rice. Plant Biotech. J. 17, 1344–1356.

    Article  CAS  Google Scholar 

  • Sanchez A. C. 1998 A gene for collarless phenotype in rice. Rice Genet. Newslett. 15, 99.

    Google Scholar 

  • Shang H., Li P., Zhang X., Xu X., Gong J., Yang S. et al. 2022 The Gain-of-function mutation, OsSpl26, positively regulates plant immunity in rice. Int. J. Mol. Sci. 23, 14168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tabuchi H., Zhang Y., Hattori S., Omae M., Shimizu-Sato S., Oikawa T. et al. 2011 LAX PANICLE2 of rice encodes a novel nuclear protein and regulates the formation of axillary meristems. Plant Cell 23, 3276–3287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi A., Kawasaki T., Henmi K., Shii K., Kodama O., Satoh H. and Shimamoto K. 1999 Lesion mimic mutants of rice with alterations in early signaling events of defense. Plant J. 17, 535–545.

    Article  CAS  PubMed  Google Scholar 

  • Tian J., Wang C., Xia J., Wu L., Xu G., Wu W. et al. 2019 Teosinte ligule allele narrows plant architecture and enhances high-density maize yields. Science 365, 658–664.

    Article  CAS  PubMed  Google Scholar 

  • Wang L., Pei Z., Tian Y. and He C. 2005 OsLSD1, a rice zinc finger protein, regulates programmed cell death and callus differentiation. Mol. Plant-Microbe Interact. 18, 375–384.

    Article  CAS  PubMed  Google Scholar 

  • Wang L., Wen R., Wang J., Xiang D., Wang Q., Zang Y. et al. 2019 Arabidopsis UBC 13 differentially regulates two programmed cell death pathways in responses to pathogen and low-temperature stress. New Phytol. 221, 919–934.

    Article  CAS  PubMed  Google Scholar 

  • Wang B., Lin Z., Li X., Zhao Y., Zhao B., Wu G. et al. 2020 Genome-wide selection and genetic improvement during modern maize breeding. Nat. Genet. 52, 565–571.

    Article  PubMed  Google Scholar 

  • Wang R., Liu C., Chen Z., Sun S. and Wang X. 2021 Oryza sativa LIGULELESS 2s determine lamina joint positioning and differentiation by inhibiting auxin signaling. New Phytol. 229, 1832–1839.

    Article  CAS  PubMed  Google Scholar 

  • Williams B. and Dickman M. 2008 Plant programmed cell death: can’t live with it; can’t live without it. Mol. Plant Pathol. 9, 531–544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H., Dai G., Yuchun R., Wu K., Wang J., Hu P. et al. 2023 Disruption of LEAF LESION MIMIC 4 affects ABA synthesis and ROS accumulation in rice. Crop J. 11, 1341–1352.

    Article  Google Scholar 

  • Xia S., Cui Y., Li F., Tan J., Xie Y., Sang X. and Ling Y. 2019 Phenotypic characterizing and gene mapping of a lesion mimic and premature senescence 1 (lmps1) mutant in rice (Oryza sativa L.). Acta Agron. Sin. 45, 46–54.

    Article  Google Scholar 

  • Xu Y., Deng M., Wu X., Bao L., Cheng J., Jing W. et al. 2010 Cloning and application of a rice liguleless gene. J. Nuclear Agric. Sci. 24, 436–441.

    CAS  Google Scholar 

  • Yamagishi J., Miyamoto N., Hirotsu S., Laza R. C. and Nemoto K. 2004 QTLs for branching, floret formation, and pre-flowering floret abortion of rice panicle in a temperate japonica× tropical japonica cross. Theor. Appl. Genet. 109, 1555–1561.

    Article  CAS  PubMed  Google Scholar 

  • Yamanouchi U., Yano M., Lin H., Ashikari M. and Yamada K. 2002 A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc. Natl. Acad. Sci. USA 99, 7530–7535.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan J., Fang Y. and Xue D. 2022 Advances in the genetic basis and molecular mechanism of lesion mimic formation in rice. Plants 11, 2169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao Y., Zhou J., Cheng C., Niu F., Zhang A., Sun B. et al. 2022 A conserved clathrin-coated vesicle component, OsSCYL2, regulates plant innate immunity in rice. Plant Cell Environ. 45, 542–555.

    Article  CAS  PubMed  Google Scholar 

  • Yin Z., Chen J., Zeng L., Goh M., Leung H., Khush G. S. and Wang G.-L. 2000 Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol. Plant-Microbe Interact. 13, 869–876.

    Article  CAS  PubMed  Google Scholar 

  • Yoshida A., Ohmori Y., Kitano H., Taguchi-Shiobara F. and Hirano H. Y. 2012 ABERRANT SPIKELET AND PANICLE1, encoding a TOPLESS-related transcriptional co-repressor, is involved in the regulation of meristem fate in rice. Plant J. 70, 327–339.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura A., Ideta O. and Iwata N. 1997 Linkage map of phenotype and RFLP markers in rice. Plant Mol. Biol. 35, 49–60.

    Article  CAS  PubMed  Google Scholar 

  • Yuchun R. A. O., Ran J., Sheng W., Xianmei W. U., Hanfei Y. E., Chenyang P. A. N. et al. 2021 SPL36 encodes a receptor-like protein kinase that regulates programmed cell death and defense responses in rice. Rice 14, 1–14.

    Article  Google Scholar 

  • Zeng L.-R., Qu S., Bordeos A., Yang C., Baraoidan M., Yan H. et al. 2004 Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16, 2795–2808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y., Liu Q., Zhang Y., Chen Y., Yu N., Cao Y. et al. 2019 LMM24 encodes receptor-like cytoplasmic kinase 109, which regulates cell death and defense responses in rice. Intl. J. Mol. Sci. 20, 3243.

    Article  CAS  Google Scholar 

  • Zhang H., Xu X., Wang M., Wang H., Deng P., Zhang Y. et al. 2021 A dominant spotted leaf gene TaSpl1 activates endocytosis and defense-related genes causing cell death in the absence of dominant inhibitors. Plant Sci. 310, 110982.

    Article  CAS  PubMed  Google Scholar 

  • Zhao M., Guo Y., Sun H., Dai J., Peng X., Wu X. et al. 2023 Lesion mimic mutant 8 balances disease resistance and growth in rice. Front. Plant Sci. 14, 1189926.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng Z., Hu H., Gao S., Zhou H., Luo W., Kage U. et al. 2022 Leaf thickness of barley: genetic dissection, candidate genes prediction and its relationship with yield-related traits. Theor. Appl. Genet. 135, 1843–1854.

    Article  CAS  PubMed  Google Scholar 

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MNM: conceptualization, methodology, data curation, formal analysis, original draft preparation and writing. KEL: methodology and editing. SGK: conceptualization, investigation, resources, visualization, supervision, writing and editing. All authors have read and agreed for the publication of the article.

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Correspondence to Sang Gu Kang.

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Ad-hoc editor: Hitendra Kumar Patel

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Matin, M.N., Lee, K.E. & Kang, S.G. Genetic characterization and linkage analysis of spotted leaf 6, liguleless and lax panicle traits in mutant rice. J Genet 103, 16 (2024). https://doi.org/10.1007/s12041-024-01466-w

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