Welcome to Acta Agronomica Sinica,

Acta Agronomica Sinica

   

Phenotype identification and gene mapping of lesion mimic and early senescence mutant lmes6 in rice

HU Yao-Jie1,LIU Ya-Ping1,ZHENG Jun-Yan1,HAN Ting1,MA Bo-Jun1,YE Ya-Feng2,LIU Bin-Mei2,*,CHEN Xi-Feng1,*   

  1. 1 College of Life Sciences, Zhejiang Normal University, Jinhua 321004, Zhejiang, China; 2 Hefei Institutes of Physical Science, Chinese Academy of Science, Hefei 230031, Anhui, China
  • Received:2024-02-05 Revised:2024-06-20 Accepted:2024-06-20 Published:2024-07-12
  • Supported by:
    This study was supported by the National Natural Science Foundation of China (32071987, 32101697, 32272096), and the Natural Science Foundation of Zhejiang Province (LQ22C130005, LZ23C130004, LZ24C130016). 

Abstract:

The occurrence of lesion mimic and early senescence is affected by multiple factors, including hormones, metabolism, and ambient signals. However, the molecular mechanism underlying this process remains incompletely understood. In this study, we identified a lesion mimic and early senescence mutant, named lmes6 (lesion mimic and early senescence 6), through screening of a heavy ion beam radiation mutagenesis library. Comparative analysis with the wild-type control revealed that the leaves of the lmes6 mutant exhibited lesion mimic, chlorosis, and a significant reduction in chlorophyll content from the tillering stage. Additionally, the mutant displayed a notable decrease in panicle length, grain number per panicle, grain length, and yield per plant. Tissue staining showed that the mutant exhibited programmed cell death and excessive accumulation of reactive oxygen species in the leaves. Furthermore, the mutant displayed enhanced resistance to bacterial blight and bacterial leaf streak. Genetic analysis showed that the mutant phenotype was governed by a single recessive nuclear gene. Through map-based cloning techniques, the gene was precisely mapped to a 53 kb region on rice chromosome 7. Candidate gene prediction and PCR sequencing analysis identified a gene, LOC_Os07g46460, which encodes Fd-GOGAT1 (ferredoxin-dependent glutamate synthase 1) in the lmes6 mutant. A single base substitution in this gene resulted in the conversion of L-phenylalanine (F) to leucine (L), which is a new multiple alleles of this gene. Interestingly, when compared to three previously reported allelic mutants—lc7abc1, and spl32, the lmes6 mutant exhibited milder growth and yield inhibition. Phylogenetic tree analysis and alignment of homologous protein sequences of Fd-GOGAT1 revealed its high conservation among monocots.

Key words: lesion mimic, early senescence, lmes6, fine mapping, sequence analysis

[1] 丁文家, 胡峻铭, 王嘉力. 水稻育种主要目标性状基因挖掘研究进展. 杂交水稻, 2023, 38(3): 1–19. 

Ding W J, Hu J M, Wang J L. Research progress on gene mining of main target traits in rice breeding. Hybrid Rice, 2023, 38(3): 1–19 (in Chinese with English abstract).

[2] Shang H H, Li P P, Zhang X B, Xu X, Gong J Y, Yang S H, He Y Q, Wu J L. The gain-of-function mutation, OsSpl26positively regulates plant immunity in rice. Int J Mol Sci, 2022, 23: 14168–14180.

[3] Zhang A P, Jiang H Z, Chu H W, Cao L M, Chen J G. Rice lesion mimic gene cloning and association analysis for disease resistance. Curr Issues Mol Biol, 2022, 44: 2350–2361.

[4] Du D, Zhang C W, Xing Y D, Lu X, Cai L J, Yun H, Zhang Q L, Zhang Y Y, Chen X L, Liu M M, Sang X C, Ling Y H, Yang Z L, Li Y F, Lefebvre B, He G H. The CC-NB-LRR OsRLR1 mediates rice disease resistance through interaction with OsWRKY19. Plant Biotechnol, 2021, 19: 1052–1064.

[5] Fan S, Wei W Q, Xiao Y Q, Qian J W, Meng F Y, Xian X D, Jin S Y. Investigating the role of OsPDCD5, a homolog of the mammalian PDCD5, in programmed cell death by inducible expression in rice. Plant Mol Biol Rep, 2012, 30: 87–98.

[6] Zeng L R, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm B H, Leung H, Wang G L. 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, 2004, 16: 2795–2808.

[7] Kojo K, Yaeno T, Kusumi K, Matsumura H, Fujisawa S, Terauchi R, Iba K. Regulatory mechanisms of ROI generation are affected by rice spl mutations. Plant Cell Physiol, 2006, 47: 1035–1044.

[8] Wang Z H, Wang Y, Hong X, Hu D H, Liu C X, Yang J, Li Y, Huang Y Q, Feng Y Q, Gong H Y, Li Y, Fang G, Tang H R, Li Y S. Functional inactivation of UDP-N-acetylglucosamine pyrophosphorylase 1 (UAP1) induces early leaf senescence and defence responses in rice. J Exp Bot, 2015, 66: 973–987.

[9] Schippers J H, Schmidt R, Wagstaff C, Jing H C. Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiol, 2015, 169: 914–930.

[10] Lee S, Masclaux-Daubresse C. Current understanding of leaf senescence in rice. Int J Mol Sci, 2021, 22: 4515–4533.

[11] Li Z, Zhang Y, Liu L, Liu Q N, Bi Z Z, Yu N, Cheng S H, Cao L Y. Fine mapping of the lesion mimic and early senescence 1 (lmes1) in rice (Oryza sativa). Plant Physiol Biochem, 2014, 80: 300–307.

[12] Xing Y D, Du D, Xiao Y H, Zhang T Q, Chen X L, Feng P, Sang X C, Wang N and He G H. Fine mapping of a new lesion mimic and early senescence 2 (lmes2) mutant in rice. Crop Sci, 2016, 56: 1550–1560.

[13] 王小虎. 水稻类病变早衰基因LMES3LMES4的克隆与功能研究. 扬州大学博士学位论文, 江苏扬州, 2018.

Wang X H. Map-based Cloning and Function Analysis of Two Lesion Mimic and Early Senescence Gene LMES3 and LMES4 in Rice. PhD Dissertation of Yang Zhou University, Yangzhou, Jiangsu, China, 2018 (in Chinese with English abstract).

[14] Han Y, Cai L J, Du D, Guo Y X, Sun H, Zhong X L, Peng X M, Dai J C, Zhang C W. Fine mapping and phenotype assessment of the novel lesion mimic and early senescence lmes5 mutant in rice. Euphytica, 2022, 218: 113.

[15] 赵晨晨, 黄福灯, 龚盼, 杨茜, 程方民, 潘刚. 水稻叶片早衰突变体osled的生理特征与基因定位. 作物学报, 2014, 40: 1946–1955.

Zhao C C, Huang F D, Gong P, Yang Q, Cheng F M, Pan G. Physiological characteristics and gene mapping of a leaf early-senescence mutant osled in rice. Acta Agron Sin, 2014, 40: 1946–1955 (in Chinese with English abstract).

[16] Christensen T H, Zhang Z G, Wei Y D, Collinge D B. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J, 1997, 11: 1187–1194.

[17] Kumar D, Yusuf M A, Singh P, Sardar M, Sarin N B. Histochemical detection of superoxide and H2O2 accumulation in Brassica juncea seedlings. Bio-Protocol, 2014, 4: 1108–1111.

[18] Porra R J, Thompson W A, Kriedemann P E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents. Biochimbiophysacta, 1989, 975: 384–394.

[19] 周永林, 申小磊, 周立帅, 林巧霞, 王朝露, 陈静, 冯慧捷, 张振文, 陈晓婷, 鲁国东. OsLOX10正调控水稻对稻瘟病和白叶枯病的抗性中国水稻科学, 2022, 36: 348–356.

Zhou Y L, Shen X L, Zhou L S, Lin Q X, Wang Z L, Chen J, Feng H J, Zhang Z W, Chen X T, Lu G D. OsLOX10 positively regulates defense responses of rice to rice blast and bacterial blight. Chin J Rice Sci, 2022, 36: 348–356 (in Chinese with English abstract).

[20] Yang B, Bogdanove A. Inoculation and virulence assay for bacterial blight and bacterial leaf streak of rice. Methods Mol Biol, 2013, 956: 249–255.

[21] 李儒剑, 万吉丽, 尹晓佳, 王克响, 米铁柱, 刘佳音, 于萌, 殷会德, 顾晓振, 李继明. SSR分子标记法快速进行常规水稻种子纯度检测的研究及应用. 杂交水稻, 2022, 37(3): 11–19.

Li R J, Wang J L, Yin X J, Wang K X, Mi T Z, Liu J Y, Yu M, Yin H D, Gu X Z, Li J M. Research and application of SSR-based method for rapid seed purity assessment of conventional rice. Hybrid Rice, 2022, 37(3): 11–19 (in Chinese with English abstract).

[22] Michelmore R W, Paran I, Kesseli R V. Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA, 1991, 88: 9828–9832.

[23] Xia Y M, Chen F S, Du Y, Liu C, Bu G H, Xin Y, Liu B Y. A modified SDS-based DNA extraction method from raw soybean. Biosci Rep, 2019, 39: 1–10.

[24] Wang Q, Chen H W, Zhu L, Feng P L, Fan M Q, Wang J Y. WSL214 negatively regulates ROS accumulation and pathogen defense response in rice. Plant Cell Rep, 2023, 42: 449–460.

[25] Liu Z Q, Zhu Y J, Shi H B, Qiu J H, Ding X H, Kou Y J. Recent progress in rice broad-spectrum disease resistance. Int J Mol Sci, 2021, 22: 11658–11674.

[26] Chen H, Li C, Liu L, Zhao J, Cheng X, Jiang G, Zhai W. The Fd-GOGAT1 mutant gene lc7 confers resistance to Xanthomonas oryzae pv. Oryzae in rice. Sci Rep, 2016, 6: 26411–26423.

[27] Chen H L, Li C R, Liu L P, Zhao J Y, Cheng X Z, Jiang G H, Zhai W X. Rice ferredoxin-dependent glutamate synthase regulates nitrogen-carbon metabolomes and is genetically differentiated between japonica and indica subspecies. Mol Plant, 2016, 9: 1520–1534.

[28] Sun L T, Wang Y H, Liu L L, Wang C M, Gan T, Zhang Z Y, Wang Y L, Wang D, Niu M, Long W H, Li X H, Zheng M, Jiang L, Wan J M. Isolation and characterization of a spotted leaf 32 mutant with early leaf senescence and enhanced defense response in rice. Sci Rep, 2017, 7: 41846–41858.

[29] Jamai A, Salome P A, Schilling S H, Weber A P, McClung C R. Arabidopsis photorespiratory serine hydroxymethyl transferase activity requires the mitochondrial accumulation of ferredoxin-dependent glutamate synthase. Plant Cell, 2009, 21: 595–606.

[30] Coschigano K T, Melo-Oliveira R, Lim J, Coruzzi G M. Arabidopsis gls mutants and distinct Fd-GOGAT genes. Implications for photorespiration and primary nitrogen assimilation. Plant Cell, 1998, 10: 741–752.

[31] 姚姝, 张亚东, 路凯, 王才林. 水稻可溶性淀粉合成酶基因SSⅡaSSⅢa的功能、等位变异及其互作研究进展. 中国水稻科学, 2022, 36: 227–236.

Yao S, Zhang Y D, Lu k, Wang C L. Progress in functions, allelic variations and interactions of soluble starch synthases genes in rice SSⅡa and SSIIIa. Chin J Rice Sci, 2022, 36: 227–236 (in Chinese with English abstract).

[1] WAN Ying-Chun, BAN Yi-Jie, JIANG Yu-Dong, WANG Ya-Xin, LIU Jing-Jing, LIU Xiao-Qing, CHENG Yu-Lin, WANG Nan, FENG Ping. Phenotypic identification and fine mapping of male sterile mutant tpa1 in rice [J]. Acta Agronomica Sinica, 2024, 50(5): 1104-1114.
[2] YU Yao, WANG Zi-Yao, ZHOU Si-Rui, LIU Peng-Cheng, YE Ya-Feng, MA Bo-Jun, LIU Bin-Mei, CHEN Xi-Feng. Phenotypic identification and disease resistance mechanism analysis of rice lesion mutant lms1 [J]. Acta Agronomica Sinica, 2024, 50(4): 857-870.
[3] ZHU Xiao-Tong, YE Ya-Feng, GUO Jun-Yao, YANG Hui-Jie, WANG Zi-Yao, ZHAN Yue, WU Yue-Jin, TAO Liang-Zhi, MA Bo-Jun, CHEN Xi-Feng, LIU Bin-Mei. Heredity and fine mapping of an early-senescence leaf gene ESL8 in rice [J]. Acta Agronomica Sinica, 2023, 49(3): 662-671.
[4] YANG Ye, SUN Qi, XING Xin-Xin, ZHANG Hai-Tao, ZHAO Zhi-Chao, CHENG Zhi-Jun. Identification of sheathed panicle mutant sui1-5 and screening of OsPSS1 interaction protein in rice (Oryza sativa L.) [J]. Acta Agronomica Sinica, 2023, 49(3): 597-607.
[5] ZHOU Wen-Qi, QIANG Xiao-Xia, LI Si-Yu, WANG Sen, WEI Wan-Rong. Identification of a rolling leaf allelic mutant e202 and fine mapping of E202 gene in rice [J]. Acta Agronomica Sinica, 2023, 49(11): 3029-3041.
[6] ZHENG Chong-Ke, ZHOU Guan-Hua, NIU Shu-Lin, HE Ya-Nan, SUN wei, XIE Xian-Zhi. Phenotypic characterization and gene mapping of an early senescence leaf H5(esl-H5) mutant in rice (Oryza sativa L.) [J]. Acta Agronomica Sinica, 2022, 48(6): 1389-1400.
[7] WANG Hao-Rang, ZHANG Yong, YU Chun-Miao, DONG Quan-Zhong, LI Wei-Wei, HU Kai-Feng, ZHANG Ming-Ming, XUE Hong, YANG Meng-Ping, SONG Ji-Ling, WANG Lei, YANG Xing-Yong, QIU Li-Juan. Fine mapping of yellow-green leaf gene (ygl2) in soybean (Glycine max L.) [J]. Acta Agronomica Sinica, 2022, 48(4): 791-800.
[8] TIAN Biao, DING Shi-Lin, LIU Chao-Lei, RUAN Ban-Pu, JIANG Hong-Zhen, GUO Rui, DONG Guo-Jun, HU Guang-Lian, GUO Long-Biao, QIAN Qian, GAO Zhen-Yu. Genetic analysis of seedling root traits and fine mapping of the QTL qLRL4 for the longest root length in rice [J]. Acta Agronomica Sinica, 2021, 47(10): 1863-1873.
[9] ZHOU Lian, LIU Chao-Xian, CHEN Qiu-Lan, WANG Wen-Qin, YAO Shun, ZHAO Zi-Kun, ZHU Si-Ying, HONG Xiang-De, XIONG Yu-Han, CAI Yi-Lin. Fine mapping and candidate gene analysis of maize defective kernel mutant dek54 [J]. Acta Agronomica Sinica, 2021, 47(10): 1903-1912.
[10] ZHANG Xue-Cui,ZHONG Chao,DUAN Can-Xing,SUN Su-Li,ZHU Zhen-Dong. Fine mapping of Phytophthora resistance gene RpsZheng in soybean cultivar Zheng 97196 [J]. Acta Agronomica Sinica, 2020, 46(7): 997-1005.
[11] REN Meng-Meng, ZHANG Hong-Wei, WANG Jian-Hua, WANG Guo-Ying, ZHENG Jun. Fine mapping of a major QTL qMES20-10 associated with deep-seeding tolerance in maize and analysis of differentially expressed genes [J]. Acta Agronomica Sinica, 2020, 46(7): 1016-1024.
[12] Li-Ping QIN,Er-Fei DONG,Yang BAI,Lian ZHOU,Lan-Yang REN,Ren-Feng ZHANG,Chao-Xian LIU,Yi-Lin CAI. Genetic analysis and molecular characterization of tasselseed mutant ts12 in maize [J]. Acta Agronomica Sinica, 2020, 46(5): 690-699.
[13] Xin-Ran SONG, Shu-Ting HU, Kai ZHANG, Ze-Jin CUI, Jian-Sheng LI, Xiao-Hong YANG, Guang-Hong BAI. Phenotypic analysis and fine mapping of dek101 in maize [J]. Acta Agronomica Sinica, 2020, 46(12): 1831-1838.
[14] SUN Qi, ZHAO Zhi-Chao, ZHANG Jin-Hui, ZHANG Feng, CHENG Zhi-Jun, ZOU De-Tang. Genetic analysis and fine mapping of a sheathed panicle mutant sui2 in rice (Oryza sativa L.) [J]. Acta Agronomica Sinica, 2020, 46(11): 1734-1742.
[15] Di JIN,Dong-Zhi WANG,Huan-Xue WANG,Run-Zhi LI,Shu-Lin CHEN,Wen-Long YANG,Ai-Min ZHANG,Dong-Cheng LIU,Ke-Hui ZHAN. Fine mapping and candidate gene analysis of awn inhibiting gene B2 in common wheat [J]. Acta Agronomica Sinica, 2019, 45(6): 807-817.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!