Abstract
Flag leaf senescence is a critical factor affecting the yield and quality of wheat. The aim of this study was to identify QTLs associated with flag leaf senescence in an F10 recombinant inbred line population derived from durum wheats UC1113 and Kofa. Bulked segregant analysis using the wheat 660K SNP array identified 3225 SNPs between extreme-phenotype bulks, and the differential SNPs were mainly clustered on chromosomes 1A, 1B, 3B, 5A, 5B, and 7A. BSR-Seq indicated that the significant SNPs were mainly located in two intervals of 354.0–389.0 Mb and 8.0–15.0 Mb on 1B and 3B, respectively. Based on the distribution of significant SNPs on chromosomes 1B and 3B, a total of 109 insertion/deletion (InDel) markers were developed, and 8 of them were finally used to map QTL in UC1113/Kofa population for flag leaf senescence. Inclusive composite interval mapping identified two major QTL in marker intervals Mar2005–Mar2116 and Mar207–Mar289, explaining 14.2–15.4% and 31.4–68.6% of the phenotypic variances across environments, respectively. Using BSR-Seq, gene expression and sequence analysis, the TraesCS1B02G211600 and TraesCS3B02G023000 were identified as candidate senescence-associated genes. This study has potential to be used in cloning key genes for flag leaf senescence and provides available molecular markers for genotyping and marker-assisted selection breeding.
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Data availability
The datasets generated during and/or analyzed during the current study are available on request.
References
Barakat M, Saleh M, Al-Doss A, Moustafa K, Elshafei A, AI-Qurainy F. (2015) Identification of new SSR markers linked to leaf chlorophyll content, flag leaf senescence and cell membrane stability traits in wheat under water stressed condition. Aust J Crop Sci. 66(1):93–102. https://doi.org/10.1556/ABiol.66.2015.1.8
Barakat MN, Wahba LE, Milad SI (2013) Molecular mapping of QTLs for wheat flag leaf senescence under water-stress. Biol Plantarum 57(1):79–84. https://doi.org/10.1007/s10535-012-0138-7
Baurley JW, Edlund CK, Pardamean CI, Conti DV, Bergen AW (2016) Smokescreen: a targeted genotyping array for addiction research. BMC Genom 17:145. https://doi.org/10.1186/s12864-016-2495-7
Beers EP, McDowell JM (2001) Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues. Curr Opin Plant Biol 4(6):561–567. https://doi.org/10.1016/S1169-5266(00)00216-8
Bi Y, Wang H, Yuan X, Yan Y, Li D, Song F (2023) The NAC transcription factor ONAC083 negatively regulates rice immunity against Magnaporthe oryzae by directly activating transcription of the RING-H2 gene OsRFPH2-6. J Integr Plant Biol 65(3):854–875. https://doi.org/10.1111/jipb.13399
Cakmak I, Pfeiffer WH, McClafferty B (2010) Biofortification of durum wheat with zinc and iron. Cereal Chem 87:10–20. https://doi.org/10.1094/CCHEM-87-1-0010
Chen F, Xu HX, Zhang FY, Xia XC, He ZH, Wang DW, Dong ZD, Zhan KH, Cheng XY, Cui DQ (2011) Physical mapping of puroindoline b-2 genes and molecular characterization of a novel variant in durum wheat (Triticum turgidum L.). Mol Breeding 28:153–161. https://doi.org/10.1007/S9032-010-9469-2
Cohen M, Hertweck K, Itkin M, Malitsky S, Dassa B, Fischer AM, Fluhr R (2022) Enhanced proteostasis, lipid remodeling, and nitrogen remobilization define barley flag leaf senescence. J Exp Bot 73(19):6816–6837. https://doi.org/10.1093/jxb/erac329
Distelfeld A, Avni R, Fischer AM (2014) Senescence, nutrient remobilization, and yield in wheat and barley. J Exp Bot 65(14):3783–3798. https://doi.org/10.1093/jxb/ert477
Dong C, Zhang L, Chen Z, Xia C, Gu Y, Wang J, Li D, Xie Z, Zhang Q, Zhang X, Gui L, Liu X, Kong X (2020) Combining a new exome capture panel with an effective varBScore algorithm accelerates BSA-based gene cloning in wheat. Front Plant Sci 11:1249. https://doi.org/10.3389/fpls.2020.01249
Dvorak J, Akhunov ED, Akhunov AR, Deal KR, Luo MC (2006) Molecular characterization of a diagnostic DNA marker for domesticated tetraploid wheat provides evidence for gene flow from wild tetraploid wheat to hexaploid wheat. Mol Biol Evol 23(7):1386–1396. https://doi.org/10.1093/molbev/msl004
Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270(5244):1986–1988. https://doi.org/10.1126/science.270.5244.1986
Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82(2):373–428. https://doi.org/10.1152/physrev.00027.2001
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
Hill JT, Demarest BL, Bisgrove BW, Gorsi B, Su YC, Yost HJ (2013) MMAPPR: mutation mapping analysis pipeline for pooled RNA-seq. Genome Res 23(4):687–697. https://doi.org/10.1101/gr.146936.112
Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53(370):927–937. https://doi.org/10.1093/jexbot/53.370.927
Hu Y, Jiang Y, Han X, Wang H, Pan J, Yu D (2017) Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. J Exp Bot 68(6):1361–1369. https://doi.org/10.1093/jxb/erx004
International Wheat Genome Sequencing Consortium (IWGSC) (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361(6403):eaar7191. https://doi.org/10.1126/science.aar7191
Kim J, Woo HR, Nam HG (2016) Toward systems understanding of leaf senescence: an integrated multi-omics perspective on leaf senescence research. Mol Plant 9(6):813–825. https://doi.org/10.1016/j.molp.2016.04.017
Lei L, Wu D, Cui C, Gao X, Yao Y, Dong J, Xu L, Yang M (2022) Transcriptome analysis of early senescence in the post-anthesis flag leaf of wheat (Triticum aestivum L.). Plants (Basel) 11(19):2593. https://doi.org/10.3390/plants11192593
Leng Y, Ye G, Zeng D (2017) Genetic dissection of leaf senescence in rice. Int J Mol Sci 18(2):2686. https://doi.org/10.3390/ijms18122686
Li H, Hua L, Rouse MN, Li T, Pang S, Bai S, Shen T, Luo J, Li H, Zhang W, Wang X, Dubcovsky J, Chen S (2021) Mapping and characterization of a wheat stem rust resistance gene in durum wheat “Kronos”. Front Plant Sci 12:751398. https://doi.org/10.3389/fpls.2021.751398
Li Q, Hu A, Qi J, Dou W, Qin X, Zou X, Xu L, Chen S, He Y (2020a) CsWAKL08, a pathogen-induced wall-associated receptor-like kinase in sweet orange, confers resistance to citrus bacterial canker via ROS control and JA signaling. Hortic Res 7:42. https://doi.org/10.1038/s41438-020-0263-y
Li Q, Hu R, Guo Z, Wang S, Gao C, Jiang Y, Tang J, Yin G (2022) SNP-based identification of QTL for resistance to black point caused by Bipolaris sorokiniana in bread wheat. Crop J 10(3):767–774. https://doi.org/10.1016/j.cj.2021.09.007
Li Z, Zhang Y, Zou D, Zhao Y, Wang HL, Zhang Y, Xia X, Luo J, Guo H, Zhang Z (2020b) LSD 3.0: a comprehensive resource for the leaf senescence research community. Nucleic Acids Res 48(D1):D1069–D1075. https://doi.org/10.1093/nar/gkz898
Liang C, Zheng G, Li W, Wang Y, Hu B, Wang H, Wu H, Qian Y, Zhu XG, Tan DX, Chen SY, Chu C (2015) Melatonin delays leaf senescence and enhances salt stress tolerance in rice. J Pineal Res 59(1):91–101. https://doi.org/10.1111/jpi.12243
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 YX, Tao Y, Wang ZQ, Guo QL, Wu FK, Yang XL, Deng M, Ma J, Chen GD, Wei YM, Zheng YL (2018) Identification of QTL for flag leaf length in common wheat and their pleiotropic effects. Mol Breed 38(1):1–11. https://doi.org/10.1007/s11032-017-0766-x
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lupton FGH (1966) Translocation of photosynthetic assimilates in wheat. Ann Appl Biol 57(3):355–364. https://doi.org/10.1111/j.1744-7348.1966.tb03829.x
Lv G, Tian Q, Zhang F, Chen J, Niaz M, Liu C, Hu H, Sun C, Chen F (2021) Reduced expression of lipoxygenase genes improves flour processing quality in soft wheat. J Exp Bot 72(18):6247–6259. https://doi.org/10.1093/jxb/erab264
Mu J, Huang S, Liu S, Zeng Q, Dai M, Wang Q, Wu J, Yu S, Kang Z, Han D (2019) Genetic architecture of wheat stripe rust resistance revealed by combining QTL mapping using SNP-based genetic maps and bulked segregant analysis. Theor Appl Genet 132(2):443–455. https://doi.org/10.1007/s00122-018-3231-2
Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10(2):79–87. https://doi.org/10.1016/j.tplants.2004.12.010
Qu X, Li C, Liu H, Liu J, Luo W, Xu Q, Tang H, Mu Y, Deng M, Pu Z, Ma J, Jiang Q, Chen G, Qi P, Jiang Y, Wei Y, Zheng Y, Lan X, Ma J (2022) Quick mapping and characterization of a co-located kernel length and thousand-kernel weight-related QTL in wheat. Theor Appl Genet 135(8):2849–2860. https://doi.org/10.1007/s00122-022-04154-4
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15(5):247–258. https://doi.org/10.1016/j.tplants.2010.02.006
Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, Innan H, Cano LM, Kamoun S, Terauchi R (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J. 74(1):174–183. https://doi.org/10.1111/tpj.12105
Uauy C, Brevis JC, Dubcovsky J (2006a) The high grain protein content gene Gpc-B1 accelerates senescence and has pleiotropic effects on protein content in wheat. J Exp Bot 57(11):2785–2794. https://doi.org/10.1093/jxb/erl047
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006b) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314(5803):1298–1301. https://doi.org/10.1126/science.1133649
Verma V, Foulkes MJ, Worland AJ, Sylvester-braldey CPDS, Snape JW (2004) Mapping quantitative trait loci for flag leaf senescence as a yield determinant in winter wheat under optimal and drought-stressed environments. Euphytica 135:255–263. https://doi.org/10.1023/B:EUPH.0000013255.31618.14
Wang D, Qin L, Wu M, Zou W, Zang S, Zhao Z, Lin P, Guo J, Wang H, Que Y (2023) Identification and characterization of WAK gene family in Saccharum and the negative roles of ScWAK1 under the pathogen stress. Int J Biol Macromol 224:1–19. https://doi.org/10.1016/j.ijbiomac.2022.11.300
Wang L, Xie X, Yao W, Wang J, Ma F, Wang C, Yang Y, Tong W, Zhang J, Xu Y, Wang X, Zhang C, Wang Y (2017) RING-H2-type E3 gene VpRH2 from Vitis pseudoreticulata improves resistance to powdery mildew by interacting with VpGRP2A. J Exp Bot 68(7):1669–1687. https://doi.org/10.1093/jxb/erx033
Wang N, Huang HJ, Ren ST, Li JJ, Sun Y, Sun DY, Zhang SQ (2012) The rice wall-associated receptor-like kinase gene OsDEES1 plays a role in female gametophyte development. Plant Physiol 160(2):696–707. https://doi.org/10.1104/pp.112.203943
Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, International Wheat Genome Sequencing Consortium, Lillemo M, Mather D et al (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12(6):787–796. https://doi.org/10.1111/pbi.12183
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
Woo HR, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death-regulation by multiple layers of control and implications for aging in general. J Cell Sci 126(21):4823–4833. https://doi.org/10.1242/jcs.109116
Woo HR, Koo HJ, Kim J, Jeong H, Yang JO, Lee IH, Jun JH, Choi SH, Park SJ, Kang B, Kim YW, Phee BK, Kim JH, Seo C, Park C, Kim SC, Park S, Lee B, Lee S et al (2016) Programming of plant leaf senescence with temporal and inter-organellar coordination of transcriptome in Arabidopsis. Plant Physiol 171(1):452–467. https://doi.org/10.1104/pp.15.01929
Xiong EH, 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(4):1–35. https://doi.org/10.1093/bib/bbaa305
Zhang HZ, Xie JZ, Chen YX, Liu X, Wang Y, Yan SH, Yang ZS, Zhao H, Wang XC, Jia LH, Cao TJ, Liu ZY (2017) Mapping stripe rust resistance gene YrZM103 in wheat cultivar Zhengmai 103 by BSR-Seq. Acta Agron Sin 43:1643–1649 (in Chinese with English abstract)
Zhang W, Chao S, Manthey F, Chicaiza O, Brevis JC, Echenique V, Dubcovsky J (2008) QTL analysis of pasta quality using a composite microsatellite and SNP map of durum wheat. Theor Appl Genet 117(8):1361–1377. https://doi.org/10.1007/s00122-008-0869-1
Zhao D, Yang L, Xu K, Cao S, Tian Y, Yan J, He Z, Xia X, Song X, Zhang Y (2020) Identification and validation of genetic loci for tiller angle in bread wheat. Theor Appl Genet 133(11):3037–3047. https://doi.org/10.1007/s00122-020-03653-6
Acknowledgements
We thank Dr. Chaonan Shi in the College of Agronomy, Henan Agricultural University, for helping in phenotypic identification.
Funding
The research was supported by the National Natural Science Foundation of China (U1904109 and 31861143008), the National Key Research and Development Program of China (2022YFD1201504 and 2019YFE0118300), Henan Major Science and Technology Project (201300111600), and Postdoctoral Science Foundation of China.
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Yan Ren: BSA-wheat 660K array and BSR-Seq analysis and writing—original draft. Xiaonan Sun, Jingyun Nie, and Xiaohui Wu: phenotyping, sampling, and marker development. Peng Guo and Yixiao Zhang: data curation and software analysis. Xia Yang, Congwei Sun, and Ning Zhang: experimental methods and guidance. Mohsin Niaz: modification language. Feng Chen: project administration, writing—review and editing, and funding acquisition.
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Ren, Y., Sun, X., Nie, J. et al. Mapping QTL conferring flag leaf senescence in durum wheat cultivars. Mol Breeding 43, 66 (2023). https://doi.org/10.1007/s11032-023-01410-3
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DOI: https://doi.org/10.1007/s11032-023-01410-3