Abstract
Main conclusion
Characterization of the early leaf senescence mutant els3 and identification of its causal gene ELS3, which encodes an LRR-RLK protein in wheat.
Abstract
Leaf senescence is an important agronomic trait that affects both crop yield and quality. However, few senescence-related genes in wheat have been cloned and functionally analyzed. Here, we report the characterization of the early leaf senescence mutant els3 and fine mapping of its causal gene ELS3 in wheat. Compared with wild-type Yanzhan4110 (YZ4110), the els3 mutant had a decreased chlorophyll content and a degraded chloroplast structure after the flowering stage. Further biochemical assays in flag leaves showed that the superoxide anion and hydrogen peroxide contents increased, while the activities of antioxidant enzymes, including catalase, superoxide dismutase and glutathione reductase, decreased gradually after the flowering stage in the els3 mutant. To clone the causal gene underlying the phenotype of leaf senescence, a genetic map was constructed using 10,133 individuals of F2:3 populations, and ELS3 was located in a 2.52 Mb region on chromosome 2DL containing 16 putative genes. Subsequent sequence analysis and gene annotation identified only one SNP (C to T) in the first exon of TraesCS2D02G332700, resulting in an amino acid substitution (Pro329Ser), and TraesCS2D02G332700 was preliminarily considered as the candidate gene of ELS3. ELS3 encodes a leucine-rich repeat receptor-like kinase (LRR-RLK) protein that is localized on the cell membrane. We also found that the transient expression of mutant TraesCS2D02G332700 can induce leaf senescence in N. benthamiana. Taken together, TraesCS2D02G332700 is likely to be the candidate gene of ELS3 and may have a function in regulating leaf senescence.
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Abbreviations
- O2 − :
-
Superoxide ions
- CAT:
-
Catalase
- DAF:
-
Day after flowering
- GR:
-
Glutathione reductase
- MDA:
-
Malondialdehyde
- SNP:
-
Single nucleotide polymorphism
- SOD:
-
Superoxide dismutase
- POD:
-
Peroxidase
References
Ahmad S, Guo Y (2019) Signal transduction in leaf senescence: progress and perspective. Plants (basel) 8(10):405. https://doi.org/10.3390/plants8100405
Ali A, Gao X, Guo Y (2018) Initiation, progression, and genetic manipulation of leaf senescence. Methods Mol Biol 1744:9–31. https://doi.org/10.1007/978-1-4939-7672-0_2
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
Buet A, Costa ML, Martínez DE, Guiamet JJ (2019) Chloroplast protein degradation in senescing leaves: proteases and lytic compartments. Front Plant Sci 10:747. https://doi.org/10.3389/fpls.2019.00747
Chen LJ, Wuriyanghan H, Zhang YQ, Duan KX, Chen HW, Li QT, Lu X, He SJ, Ma B, Zhang WK, Lin Q, Chen SY, Zhang JS (2013) An S-domain receptor-like kinase OsSIK2 confers abiotic stress tolerance and delays dark-induced leaf senescence in rice. Plant Physiol 163(4):1752–1765. https://doi.org/10.1104/pp.113.224881
Chen Z, Wang Y, Huang R, Zhang Z, Huang J, Yu F, Lin Y, Guo Y, Liang K, Zhou Y, Chen F (2022) Integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in rice. BMC Plant Biol 22(1):137. https://doi.org/10.1186/s12870-022-03510-2
Diaz-Mendoza M, Velasco-Arroyo B, Santamaria ME, González-Melendi P, Martinez M, Diaz I (2016) Plant senescence and proteolysis: two processes with one destiny. Genet Mol Biol 39:329–338. https://doi.org/10.1590/1678-4685-GMB-2016-0015
Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101. https://doi.org/10.1002/bies.20493
Guo Y, Gan S (2005) Leaf senescence: signals, execution, and regulation. Curr Top Dev Biol 71:83–112. https://doi.org/10.1016/S0070-2153(05)71003-6
Guo Y, Gan SS (2012) Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ 35:644–655. https://doi.org/10.1111/j.1365-3040.2011.02442.x
Havé M, Marmagne A, Chardon F, Masclaux-Daubresse C (2017) Nitrogen remobilization during leaf senescence: lessons from Arabidopsis to crops. J Exp Bot 68:2513–2529. https://doi.org/10.1093/jxb/erw365
Hu C, Zhu Y, Cui Y, Cheng K, Liang W, Wei Z, Zhu M, Yin H, Zeng L, Xiao Y, Lv M, Yi J, Hou S, He K, Li J, Gou X (2018) A group of receptor kinases are essential for clavata signaling to maintain stem cell homeostasis. Nat Plants 4:205–211. https://doi.org/10.1038/s41477-018-0123-z
Hussain A, Shah F, Ali F, Yun BW (2022) Role of nitric oxide in plant senescence. Front Plant Sci 13:851631. https://doi.org/10.3389/fpls.2022.851631
Jajic I, Sarna T, Strzalka K (2015) Senescence, stress, and reactive oxygen species. Plants (basel) 4(3):393–411. https://doi.org/10.3390/plants4030393
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
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Lee S, Masclaux-Daubresse C (2021) Current understanding of leaf senescence in rice. Int J Mol Sci 22:4515. https://doi.org/10.3390/ijms22094515
Lee IC, Hong SW, Whang SS, Lim PO, Nam HG, Koo JC (2011) Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves. Plant Cell Physiol 52:651–662. https://doi.org/10.1093/pcp/pcr026
Li X, Li JH, Wang W, Chen NZ, Ma TS, Xi YN, Zhang XL, Lin HF, Bai Y, Huang SJ, Chen YL (2014) Arp2/3 complex-mediated actin dynamics is required for hydrogen peroxide-induced stomatal closure in Arabidopsis. Plant Cell Environ 37:1548–1560
Li M, Li B, Guo G, Chen Y, Xie J, Lu P, Wu Q, Zhang D, Zhang H, Yang J (2018) Mapping a leaf senescence gene els1 by BSR-seq in common wheat. Crop J 6:236–243. https://doi.org/10.1016/j.cj.2018.01.004
Li X, Ahmad S, Ali A, Guo C, Li H, Yu J, Zhang Y, Gao X, Guo Y (2019) Characterization of somatic embryogenesis receptor-like kinase 4 as a negative regulator of leaf senescence in Arabidopsis. Cells 8:50. https://doi.org/10.3390/cells8010050
Liang C, Wang Y, Zhu Y, Tang J, Hu B, Liu L, Ou S, Wu H, Sun X, Chu J, Chu C (2014) OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc Natl Acad Sci USA 111:10013–10018. https://doi.org/10.1073/pnas.1321568111
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
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods (san Diego, Calif.) 25:402–408. https://doi.org/10.1006/meth.2001.1262
Maillard A, Diquélou S, Billard V, Laîné P, Garnica M, Prudent M, Garcia-Mina JM, Yvin JC, Ourry A (2015) Leaf mineral nutrient remobilization during leaf senescence and modulation by nutrient deficiency. Front Plant Sci 6:317. https://doi.org/10.3389/fpls.2015.00317
Matsuoka D, Yasufuku T, Furuya T, Nanmori T (2015) An abscisic acid inducible Arabidopsis MAPKKK MAPKKK18 regulates leaf senescence via its kinase activity. Plant Mol Biol 87(6): 565–575. https://doi.org/10.1007/s11103-015-0295-0
Nakagawa T, Suzuki T, Murata S, Nakamura S, Hino T, Maeo K, Tabata R, Kawai T, Tanaka K, Niwa Y, Watanabe Y, Nakamura K, Kimura T, Ishiguro S (2007) Improved gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci Biotechnol Biochem 71(8):2095–2100. https://doi.org/10.1271/bbb.70216
Sade N, Del Mar R-W, Umnajkitikorn K, Blumwald E (2018) Stress-induced senescence and plant tolerance to abiotic stress. J Exp Bot 69:845–853. https://doi.org/10.1093/jxb/erx235
Shin D, Lee S, Kim TH, Lee JH, Park J, Lee J, Lee JY, Cho LH, Choi JY, Lee W, Park JH, Lee DW, Ito H, Kim DH, Tanaka A, Cho JH, Song YC, Hwang D, Purugganan MD, Jeon JS, An G, Nam HG (2020) Natural variations at the stay-green gene promoter control lifespan and yield in rice cultivars. Nat Commun 11:2819. https://doi.org/10.1038/s41467-020-16573-2
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Plant J 11:1187–1194. https://doi.org/10.1046/j.1365-313X.1997.11061187.x
Wang N, Xie Y, Li Y, Wu S, Li S, Guo Y, Wang C (2020) High-resolution mapping of the novel early leaf senescence gene els2 in common wheat. Plants (basel) 9:698. https://doi.org/10.3390/plants9060698
Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie AR, Hoefgen R (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol 162:1290–1310. https://doi.org/10.1104/pp.113.217380
Woo HR, Kim HJ, Lim PO, Nam HG (2019) Leaf senescence: systems and dynamics aspects. Annu Rev Plant Biol 70:347–376. https://doi.org/10.1146/annurev-arplant-050718-095859
Xiong E, Li Z, Zhang C, Zhang J, Liu Y, Peng T, Chen Z, Zhao Q (2021) A study of leaf-senescence genes in rice based on a combination of genomics, proteomics and bioinformatics. Brief Bioinform 22:305. https://doi.org/10.1093/bib/bbaa305
Xu F, Meng T, Li P, Yu Y, Cui Y, Wang Y, Gong Q, Wang NN (2011) A soybean dual-specificity kinase, GmSARK, and its Arabidopsis homolog, AtSARK, regulate leaf senescence through synergistic actions of auxin and ethylene. Plant Physiol 157:2131–2153. https://doi.org/10.1104/pp.111.182899
Xu J, Wang C, Wang F, Liu Y, Li M, Wang H, Zheng Y, Zhao K, Ji Z (2023) PWL1, a G-type lectin receptor-like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice. Plant Biotechnol J. https://doi.org/10.1111/pbi.14150. (Advance online publication)
Yang S, Fang G, Zhang A, Ruan B, Jiang H, Ding S, Liu C, Zhang Y, Jaha N, Hu P, Xu Z, Gao Z, Wang J, Qian Q (2020a) Rice EARLY SENESCENCE 2, encoding an inositol polyphosphate kinase, is involved in leaf senescence. BMC Plant Biol 20:393. https://doi.org/10.1186/s12870-020-02610-1
Yang Z, Wang C, Qiu K, Chen H, Li Z, Li X, Song J, Wang X, Gao J, Kuai B, Zhou X (2020b) The transcription factor ZmNAC126 accelerates leaf senescence downstream of the ethylene signaling pathway in maize. Plant Cell Environ 43:2287–2300. https://doi.org/10.1111/pce.13803
Zhang Q, Xia C, Zhang L, Dong C, Liu X, Kong X (2018a) Transcriptome analysis of a premature leaf senescence mutant of common wheat (Triticum aestivum L.). Int J Mol Sci 19:782. https://doi.org/10.3390/ijms19030782
Zhang Z, Liu C, Li K, Li X, Xu M, Guo Y (2022) CLE14 functions as a “brake signal” to suppress age-dependent and stress-induced leaf senescence by promoting JUB1-mediated ROS scavenging in Arabidopsis. Mol Plant 15:179–188. https://doi.org/10.1016/j.molp.2021.09.006
Zhang X, Liu G, Zhang L, Xia C, Zhao T, Jia J, Liu X, Kong X (2018) Fine mapping of a novel heading date gene, TaHdm605, in hexaploid wheat. Front Plant Sci 9: 1059. https://doi.org/10.3389/fpls.2018.01059
Zheng X, Fan S, Wei H, Tao C, Ma Q, Ma Q, Zhang S, Li H, Pang C, Yu S (2017) iTRAQ-based quantitative proteomic analysis reveals cold responsive proteins involved in leaf senescence in upland cotton (Gossypium hirsutum L.). Int J Mol Sci 18:1984. https://doi.org/10.3390/ijms18091984
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This work was supported by the National Natural Science Foundation of China (31971878).
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ZX and QZ conceived of the project; XL, XK and LZ designed the experiments; CX, CD and DL identified and characterized the mutant; ZX, QZ and LZ analyzed the data; ZX, QZ, XL, XK and LZ wrote the manuscript; and all the authors have read and approved the final manuscript.
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Xie, Z., Zhang, Q., Xia, C. et al. Identification of the early leaf senescence gene ELS3 in bread wheat (Triticum aestivum L.). Planta 259, 5 (2024). https://doi.org/10.1007/s00425-023-04278-x
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DOI: https://doi.org/10.1007/s00425-023-04278-x