Abstract
Lesion mimic mutants spontaneously produce necrotic lesions similar to hypersensitive response in the absence of external stress. In this study, a novel lesion mimic and early senescence 5 (lmes5) mutant was identified after ethyl methanesulfonate mutagenesis. The mutant showed premature ageing at the mature stage, as well as the localized necrosis phenotype. Leaves of the lmes5 mutant showed decreased chlorophyll fluorescence, photosynthetic pigment contents, and net photosynthetic rate. In contrast, there was an increase in the number of dead cells, an accumulation of reactive oxygen species (hydrogen peroxide and hydroxyl radical), and decreased activities of superoxide dismutase and peroxidase. Consistent with these physiological changes, agronomic traits of the lmes5 mutant, such as plant height, percentage seed set, 1000-grain weight, and number of grains per panicle, were reduced. Consistent with the lesion mimic phenotype, there was an increase in expression of antioxidant reaction-related genes, and pathogenesis-related genes. Resistance to bacterial blight was enhanced and the spectrum of resistance to rice blast was broadened. In accordance with the phenotype of premature senescence, genes associated with chlorophyll synthesis and chloroplast development were inhibited, whereas genes associated with chlorophyll degradation were activated. Fine mapping revealed that the mutated gene was localized within a 116 kb interval on chromosome 4. At present, no lesion mimic genes have been reported in this region.
Similar content being viewed by others
Abbreviations
- EMS:
-
Ethyl methanesulfonate
- POD:
-
Peroxidase
- T-SOD:
-
Total superoxide dismutase
- PCD:
-
Programmed cell death
- WT:
-
Wild type
- DAB:
-
Diaminbenzine
- ROS:
-
Reactive oxygen species
- MDA:
-
Malondialdehyde
- H2O2 :
-
Hydrogen peroxide
- .OH:
-
Hydroxyl radical
References
All China Coorporation of Research on Physiological Races of Pyricularia oryzae (1980) Research on physiological races of rice blast fungus in China. Acta Phytopathol Sin 10:71–82 ((in Chinese))
Badigannavar AM, Kale DM, Eapen S, Murty GSS (2002) Inheritance of disease lesion mimic leaf trait in groundnut. J Hered 93:50–52. https://doi.org/10.1093/jhered/93.1.50
Chen X, Jia Y, Jia MH, Pinson SRM, Wang X, Wu BM (2018) Functional interactions between major rice blast resistance genes, Pi-ta and Pi-b, and minor blast resistance quantitative trait loci. Phytopathology 108:1095–1103. https://doi.org/10.1094/PHYTO-02-18-0032-R
Elmore S (2007) Apoptosis: A review of programmed cell death. Toxicol Pathol 35:495–516. https://doi.org/10.1080/01926230701320337
Gu K, Tian D, Yang F, Wu L, Sreekala C, Wang D, Wang GL, Yin Z (2004) High-resolution genetic mapping of Xa27(t), a new bacterial blight resistance gene in rice. Oryza Sativa l Theor Appl Genet 108:800–807. https://doi.org/10.1007/s00122-003-1491-x
Herrera-Vásquez A, Salinas P, Holuigue L (2015) Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front Plant Sci 6:171. https://doi.org/10.3389/fpls.2015.00171
Hoisington DA, Neuffer MG, Walbot V (1982) Disease lesion mimics in maize. I. Effect of genetic background, temperature, developmental age, and wounding on necrotic spot formation with Les1. Dev Biol 93:381–388. https://doi.org/10.1016/0012-1606(82)90125-7
Hu G, Yalpani N, Briggs SP, Johal GS (1998) A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10:1095–1105. https://doi.org/10.1105/tpc.10.7.1095
Jambunathan N, McNellis TW (2003) Regulation of Arabidopsis COPINE 1 gene expression in response to pathogens and abiotic stimuli. Plant Physiol 132:1370–1381. https://doi.org/10.1104/pp.103.022970
Jiao BB, Wang JJ, Zhu XD, Zeng LJ, Li Q, He ZH (2012) A novel protein RLS1 with NB-ARM domains is involved in chloroplast degradation during leaf senescence in rice. Mol Plant 5:205–217. https://doi.org/10.1093/mp/ssr081
Koch E, Slusarenko A (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2:437–444. https://doi.org/10.1105/tpc.2.5.437
Landoni M, Francesco AD, Bellatti S, Delledonne M, Ferrarini A, Venturini L, Pilu R, Bononi M (2013) Chiara Tonelli A mutation in the FZL gene of Arabidopsis causing alteration in chloroplast morphology results in a lesion mimic phenotype. J Exp Bot 64:4313–4328. https://doi.org/10.1093/jxb/ert237
Li R, Afsheen S, Xin Z, Han X, Lou Y (2013) OsNPR1 negatively regulates herbivore-induced JA and ethylene signaling and plant resistance to a chewing herbivore in rice. Physiol Plant 147:340–351. https://doi.org/10.1111/j.1399-3054.2012.01666.x
Li Z, Zhang Y, Liu L, Liu Q, Bi Z, Yu N, Cheng S, Cao L (2014) Fine mapping of the lesion mimic and early senescence 1 (lmes1) in rice (Oryza sativa). Plant Physiol Biochem 80:300–307. https://doi.org/10.1016/j.plaphy.2014.03.031
Li Z, Mo W, Jia L, Xu YC, Tang W, Yang W, Guo YL, Lin R (2019) Rice FLUORESCENT1 is involved in the regulation of chlorophyll. Plant Cell Physiol 60:2307–2318. https://doi.org/10.1093/pcp/pcz129
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136. https://doi.org/10.1146/annurev.arplant.57.032905.105316
Liu J, Park CH, He F, Nagano M, Wang M, Bellizzi M, Zhang K, Zeng X, Liu W, Ning Y, Kawano Y, Wang GL (2015) The RhoGAP SPIN6 associates with SPL11 and OsRac1 and negatively regulates programmed cell death and innate immunity in rice. Plos Pathog 11:e1004629. https://doi.org/10.1371/journal.ppat.1004629
Lorrain S, Vailleau F, Balagué C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8:263–271. https://doi.org/10.1016/S1360-1385(03)00108-0
Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549. https://doi.org/10.1038/ng.592
Molina A, Volrath S, Guyer D, Maleck K, Ryals J, Ward E (1999) Inhibition of protoporphyrinogen oxidase expression in Arabidopsis causes a lesion-mimic phenotype that induces systemic acquired resistance. Plant J 17:667–678. https://doi.org/10.1046/j.1365-313x.1999.00420.x
Morris K, MacKerness SA, Page T, John CF, Murphy AM, Carr JP, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J 23:677–685. https://doi.org/10.1046/j.1365-313x.2000.00836.x
Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P (2002) The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli1. Plant Physiol 129:1076–1085. https://doi.org/10.1104/pp.010954
Pitsili E, Phukan UJ, Coll NS (2020) Cell Death in Plant Immunity. Cold Spring Harb Perspect Biol 12:a036483. https://doi.org/10.1101/cshperspect.a036483
Qiao Y, Jiang W, Lee JH, Park BS, Choi MS, Piao R, Woo MO, Roh JH, Han L, Paek NC, Seo HS, Koh HJ (2010) SPL28 encodes a clathrin-associated adaptor protein complex 1, medium subunit l1 (AP1M1) and is responsible for spotted leaf and early senescence in rice (Oryza sativa). New Phytol 185:258–274. https://doi.org/10.1111/j.1469-8137.2009.03047.x
Quirino BF, Normanly J, Amasino RM (1999) Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol Biol 40:267–278. https://doi.org/10.1023/a:1006199932265
Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16:1139–1149. https://doi.org/10.1101/gad.222702
Takahashi A, Kawasaki T, Henmi K, ShiI K, Kodama O, Satoh H, Shimamoto K (1999) Lesion mimic mutants of rice with alterations in early signaling events of defense. Plant J 17:535–545. https://doi.org/10.1046/j.1365-313x.1999.00405.x
Tamiru M, Takagi H, Abe A, Yokota T, Kanzaki H, Okamoto H, Saitoh H, Takahashi H, Fujisaki K, Oikawa K, Uemura A, Natsume S, Jikumaru Y, Matsuura H, Umemura K, Terry MJ, Terauchi R (2016) A chloroplast-localized protein LESION AND LAMINA BENDING affects defence and growth responses in rice. New Phytol 210:1282–1297. https://doi.org/10.1111/nph.13864
Tang J, Wang Y, Yin W, Dong G, Sun K, Teng Z, Wu X, Wang S, Qian Y, Pan X, Qian Q, Chu C (2019) Mutation of a Nucleotide-Binding Leucine-Rich Repeat immune receptor-type protein disrupts immunity to bacterial blight. Plant Physiol 181:1295–1313. https://doi.org/10.1104/pp.19.00686
Tong X, Qi J, Zhu X, Mao B, Zeng L, Wang B, Li Q, Zhou G, Xu X, Lou Y, He Z (2012) The rice hydroperoxidelyase OsHPL3 functions in defense responses by modulating the oxylipin pathway. Plant J 71:763–775. https://doi.org/10.1111/j.1365-313X.2012.05027.x
Undan JR, Tamiru M, Abe A, Yoshida K, Kosugi S, Takagi H, Yoshida K, Kanzaki H, Saitoh H, Fekih R, Sharma S, Undan J, Yano M, Terauchi R (2012) Mutation in OsLMS, a gene encoding a protein with two double-stranded RNA binding motifs, causes lesion mimic phenotype and early senescence in rice (Oryza sativa L.). Genes Genet Syst 87:169–179. https://doi.org/10.1266/ggs.87.169
Vanacker H, Carver TL, Foyer CH (2000) Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley-powdery mildew interaction. Plant Physiol 123:1289–1300. https://doi.org/10.1104/pp.123.4.1289
Vega-Sánchez ME, Zeng L, Chen S, Leung H, Wang G (2008) Spin1, a k homology domain protein negatively regulated and ubiquitinated by the e3 ubiquitin ligase spl11, is involved in flowering time control in rice. Plant Cell 20:1456–1469. https://doi.org/10.1105/tpc.108.058610
Wang Y, Li J (2011) Branching in rice. Curr Opin Plant Biol 14:94–99. https://doi.org/10.1016/j.pbi.2010.11.002
Wang L, Pei Z, Tian Y, He C (2005) OsLSD1, a rice zinc finger protein, regulates programmed cell death and callus differentiation. Mol Plant Microbe Interact 18:375–384. https://doi.org/10.1094/MPMI-18-0375
Wang Z, Wang Y, Hong X, Hu D, Liu C, Yang J, Li Y, Huang Y, Feng Y, Gong H, Li Y, Fang G, Tang H, Li Y (2015a) Functional inactivation of udp-N-acetylglucosamine pyrophosphorylase 1 (uap1) induces early leaf senescence and defence responses in rice. J Exp Bot 66:973–987. https://doi.org/10.1093/jxb/eru456
Wang J, Zhou L, Shi H, Wang J, Zhou L, Shi H, Chern M, Yu H, Yi H, He M, Yin J, Zhu X, Li Y, Li W, Liu J, Wang J, Chen X, Qing H, Wang Y, Liu G, Wang W, Li P, Wu X, Zhu L, Zhou JM, Ronald PC, Li S, Li J, Chen X (2018) A single transcription factor promotes both yield and immunity in rice. Science 361:1026–1028. https://doi.org/10.1126/science.aat7675
Wang J, Liu X, Zhang A, RenY WuF, Wang G, Xu Y, Lei C, Zhu S, Pan T, Wang Y, Zhang H, Wang F, Tan YQ, Wang Y, Jin X, Luo S, Zhou C, Zhang X, Liu J, Wang S, Meng L, Wang Y, Chen X, Lin Q, Zhang X, Guo X, Cheng Z, Wang J, Tian Y, Liu S, Jiang L, Wu C, Wang E, Zhou JM, Wang YF, Wang H, Wan J (2019) A cyclic nucleotide-gated channel mediates cytoplasmic calcium elevation and disease resistance in rice. Cell Res 29:820–831. https://doi.org/10.1038/s41422-019-0219-7
Wang J, Ye B, Yin J, Yuan C, Zhou X, Li W, He M, Wang J, Chen W, Qin P, Ma B, Wang Y, Li S, Chen X (2015b) Characterization and fine mapping of a light-dependent leaf lesion mimic mutant 1 in rice. Plant Physiol Biochem 97:44–51. https://doi.org/10.1016/j.plaphy.2015b.09.001
Woo HR, Masclaux-Daubresse C, Lim PO (2018) Plant senescence: how plants know when and how to die. J Exp Bot 69:715–718. https://doi.org/10.1093/jxb/ery011
Yang X, Gong P, Li K, Huang F, Cheng F, Pan G (2016) A single cytosine deletion in the OsPLS1 gene encoding vacuolar-type H+-ATPase subunit A1 leads to premature leaf senescence and seed dormancy in rice. J Exp Bot 67:2761–2776. https://doi.org/10.1093/jxb/erw109
Zhang Z, Zhang Q, Wu J, Zheng X, Zheng S, Sun X, Qiu Q, Lu T (2013) Gene knockout study reveals that cytosolic ascorbate peroxidase 2 (Osapx2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses. PLoS ONE 8:e57472. https://doi.org/10.1371/journal.pone.0057472
Funding
This work was supported by grants from the Chongqing Technology Innovation and Application demonstration project(cstc2018jscx-msybX0250).
Author information
Authors and Affiliations
Contributions
Changwei Zhang conceived and designed the research. Han Yun, Linjun Cai, Dan Du, Yunxia Guo, Hang Sun, Xiaolong Zhong, Ximan Peng, Jichao Dai and Changwei Zhang assisted in the experiments. Han Yun and Linjun Cai analyzed the experimental data and wrote the manuscript. HanYun and Linjun Cai contributed equally. All authors discussed the results and commented on the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that there are no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yun, H., Cai, L., Du, D. et al. Fine mapping and phenotype assessment of the novel lesion mimic and early senescence lmes5 mutant in rice. Euphytica 218, 45 (2022). https://doi.org/10.1007/s10681-022-02991-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10681-022-02991-4