Identification of Sclerotinia stem rot resistance quantitative trait loci in a chickpea (Cicer arietinum) recombinant inbred line population
Virginia W. Mwape A B , Kelvin H. P. Khoo C , Kefei Chen D , Yuphin Khentry A , Toby E. Newman A , Mark C. Derbyshire A , Diane E. Mather C and Lars G. Kamphuis A B *A Centre for Crop Disease Management, Curtin University, Bentley, WA 6102, Australia.
B Commonwealth Scientific and Industrial Research Organization, Agriculture and Food, Floreat, WA 6913, Australia.
C School of Agriculture, Food and Wine, Waite Research Institute, University of Adelaide, Urrbrae, SA 5064, Australia.
D Statistics for the Australian Grains Industry - West, Curtin University, Bentley, WA 6102, Australia.
Functional Plant Biology 49(7) 634-646 https://doi.org/10.1071/FP21216
Submitted: 29 July 2021 Accepted: 4 March 2022 Published: 28 March 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Sclerotinia stem rot (SSR), caused by Sclerotinia sclerotiorum, is one of the most economically devastating diseases in chickpea (Cicer arietinum L.). No complete resistance is available in chickpea to this disease, and the inheritance of partial resistance is not understood. Two hundred F7 recombinant inbred lines (RILs) derived from a cross between a partially resistant variety PBA HatTrick, and a highly susceptible variety Kyabra were characterised for their responses to SSR inoculation. Quantitative trait locus (QTL) analysis was conducted for the area under the disease progress curve (AUDPC) after RIL infection with S. sclerotiorum. Four QTLs on chromosomes, Ca4 (qSSR4-1, qSSR4-2), Ca6 (qSSR6-1) and Ca7 (qSSR7-1), individually accounted for between 4.2 and 15.8% of the total estimated phenotypic variation for the response to SSR inoculation. Candidate genes located in these QTL regions are predicted to be involved in a wide range of processes, including phenylpropanoid biosynthesis, plant-pathogen interaction, and plant hormone signal transduction. This is the first study investigating the inheritance of resistance to S. sclerotiorum in chickpea. Markers associated with the identified QTLs could be employed for marker-assisted selection in chickpea breeding.
Keywords: chickpea, disease resistance, Fabaceae, legume, polygenic disease resistance, quantitative trait locus analysis, Sclerotinia stem rot, Sclerotinia white mold.
References
Abbo S, Berger J, Turner NC (2003) Viewpoint: Evolution of cultivated chickpea: four bottlenecks limit diversity and constrain adaptation. Functional Plant Biology 30, 1081–1087.| Viewpoint: Evolution of cultivated chickpea: four bottlenecks limit diversity and constrain adaptation.Crossref | GoogleScholarGoogle Scholar | 32689090PubMed |
Ali S, Ganai BA, Kamili AN, Bhat AA, Mir ZA, Bhat JA, Tyagi A, Islam ST, Mushtaq M, Yadav P, Rawat S, Grover A (2018) Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiological Research 212–213, 29–37.
| Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance.Crossref | GoogleScholarGoogle Scholar | 29853166PubMed |
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
| Basic local alignment search tool.Crossref | GoogleScholarGoogle Scholar | 2231712PubMed |
Anuradha C, Gaur PM, Pande S, Gali KK, Ganesh M, Kumar J, Varshney RK (2011) Mapping QTL for resistance to botrytis grey mould in chickpea. Euphytica 182, 1–9.
| Mapping QTL for resistance to botrytis grey mould in chickpea.Crossref | GoogleScholarGoogle Scholar |
Arahana VS, Graef GL, Specht JE, Steadman JR, Eskridge KM (2001) Identification of QTLs for resistance to Sclerotinia sclerotiorum in soybean. Crop Science 41, 180–188.
| Identification of QTLs for resistance to Sclerotinia sclerotiorum in soybean.Crossref | GoogleScholarGoogle Scholar |
Ashtari Mahini R, Kumar A, Elias EM, Fiedler JD, Porter LD, McPhee KE (2020) Analysis and identification of QTL for resistance to Sclerotinia sclerotiorum in pea (Pisum sativum L.). Frontiers in Genetics 11, 587968
| Analysis and identification of QTL for resistance to Sclerotinia sclerotiorum in pea (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar | 33329732PubMed |
Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer ELL (2002) The Pfam protein families database. Nucleic Acids Research 30, 276–280.
| The Pfam protein families database.Crossref | GoogleScholarGoogle Scholar | 11752314PubMed |
Bohra A, Pandey MK, Jha UC, Singh B, Singh IP, Datta D, Chaturvedi SK, Nadarajan N, Varshney RK (2014) Genomics-assisted breeding in four major pulse crops of developing countries: present status and prospects. Theoretical and Applied Genetics 127, 1263–1291.
| Genomics-assisted breeding in four major pulse crops of developing countries: present status and prospects.Crossref | GoogleScholarGoogle Scholar | 24710822PubMed |
Boland GJ, Hall R (1994) Index of plant hosts of Sclerotinia sclerotiorum. Canadian Journal of Plant Pathology 16, 93–108.
| Index of plant hosts of Sclerotinia sclerotiorum.Crossref | GoogleScholarGoogle Scholar |
Brien C (2021) Employing asremlPlus, in conjunction with asreml, to calculate and use information criteria. Available at https://cran.r-project.org/web/packages/asremlPlus/vignettes
Brooks KD, Bennett SJ, Hodgson LM, Ashworth MB (2018) Narrow windrow burning canola (Brassica napus L.) residue for Sclerotinia sclerotiorum (Lib.) de Bary sclerotia destruction. Pest Management Science 74, 2594–2600.
| Narrow windrow burning canola (Brassica napus L.) residue for Sclerotinia sclerotiorum (Lib.) de Bary sclerotia destruction.Crossref | GoogleScholarGoogle Scholar | 29687565PubMed |
Butler DG, Cullis BR, Gilmour AR, Gogel BJ, Thompson, R (2018) ‘ASReml-R reference manual version 4.’ (VSN International Ltd, Hemel Hempstead, HPI 1ES, UK)
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. The Plant Journal 3, 1–30.
| Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth.Crossref | GoogleScholarGoogle Scholar | 8401598PubMed |
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138, 963–971.
| Empirical threshold values for quantitative trait mapping.Crossref | GoogleScholarGoogle Scholar | 7851788PubMed |
Denton-Giles M, Derbyshire MC, Khentry Y, Buchwaldt L, Kamphuis LG (2018) Partial stem resistance in Brassica napus to highly aggressive and genetically diverse Sclerotinia sclerotiorum isolates from Australia. Canadian Journal of Plant Pathology 40, 551–561.
| Partial stem resistance in Brassica napus to highly aggressive and genetically diverse Sclerotinia sclerotiorum isolates from Australia.Crossref | GoogleScholarGoogle Scholar |
Deokar A, Sagi M, Daba K, Tar’an B (2019) QTL sequencing strategy to map genomic regions associated with resistance to ascochyta blight in chickpea. Plant Biotechnology Journal 17, 275–288.
| QTL sequencing strategy to map genomic regions associated with resistance to ascochyta blight in chickpea.Crossref | GoogleScholarGoogle Scholar | 29890030PubMed |
Dey SK, Singh G (1993) Resistance to ascochyta blight in chickpea – Genetic basis. Euphytica 68, 147–153.
| Resistance to ascochyta blight in chickpea – Genetic basis.Crossref | GoogleScholarGoogle Scholar |
Dmochowska-Boguta M, Nadolska-Orczyk A, Orczyk W (2013) Roles of peroxidases and NADPH oxidases in the oxidative response of wheat (Triticum aestivum) to brown rust (Puccinia triticina) infection. Plant Pathology 62, 993–1002.
Edwards D (2016) ‘Improved kabuli reference genome.’ (CyVerse Data Commons)
| Crossref |
Ender M, Kelly JD (2005) Identification of QTL associated with white mold resistance in common bean. Crop Science 45, 2482–2490.
| Identification of QTL associated with white mold resistance in common bean.Crossref | GoogleScholarGoogle Scholar |
FAOSTAT (2019) Food and agriculture data. Available at http://www.fao.org.dbgw.lis.curtin.edu.au/faostat/en/ [Accessed 29 May 2020]
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Research 42, D222–D230.
| Pfam: the protein families database.Crossref | GoogleScholarGoogle Scholar | 24288371PubMed |
Fuhlbohm MJ, Tatnell JR, Ryley MJ (2003) First report of stem rot and wilt of chickpea caused by Sclerotinia minor in Queensland, Australia. Australasian Plant Pathology 32, 323–324.
| First report of stem rot and wilt of chickpea caused by Sclerotinia minor in Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Garg T, Mallikarjuna BP, Thudi M, Samineni S, Singh S, Sandhu JS, Kaur L, Singh I, Sirari A, Basandrai AK, Basandrai D, Varshney RK, Gaur PM (2018) Identification of QTLs for resistance to Fusarium wilt and Ascochyta blight in a recombinant inbred population of chickpea (Cicer arietinum L.). Euphytica 214, 45
| Identification of QTLs for resistance to Fusarium wilt and Ascochyta blight in a recombinant inbred population of chickpea (Cicer arietinum L.).Crossref | GoogleScholarGoogle Scholar |
Gaur PM, Jukanti AK, Varshney RK (2012) Impact of genomic technologies on chickpea breeding strategies. Agronomy 2, 199–221.
| Impact of genomic technologies on chickpea breeding strategies.Crossref | GoogleScholarGoogle Scholar |
Jeger MJ, Viljanen-Rollinson SLH (2001) The use of the area under the disease-progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars. Theoretical and Applied Genetics 102, 32–40.
| The use of the area under the disease-progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars.Crossref | GoogleScholarGoogle Scholar |
Jha UC, Chaturvedi SK, Bohra A, Basu PS, Khan MS, Barh D (2014) Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breeding 133, 163–178.
| Abiotic stresses, constraints and improvement strategies in chickpea.Crossref | GoogleScholarGoogle Scholar |
Jiang M, Ye Z, Zhang H, Miao L (2019) Broccoli plants over-expressing an ERF transcription factor gene BoERF1 facilitates both salt stress and Sclerotinia stem rot resistance. Journal of Plant Growth Regulation 38, 1–13.
| Broccoli plants over-expressing an ERF transcription factor gene BoERF1 facilitates both salt stress and Sclerotinia stem rot resistance.Crossref | GoogleScholarGoogle Scholar |
Jukanti AK, Gaur PM, Gowda CLL, Chibbar RN (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. British Journal of Nutrition 108, S11–S26.
| Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review.Crossref | GoogleScholarGoogle Scholar |
Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53, 983–997.
| Small sample inference for fixed effects from restricted maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 9333350PubMed |
Khoo KHP, Sheedy JG, Taylor JD, Croser JS, Hayes JE, Sutton T, Thompson JP, Mather DE (2021) A QTL on the Ca7 chromosome of chickpea afects resistance to the root-lesion nematode Pratylenchus thornei. Molecular Breeding 41, 78
| A QTL on the Ca7 chromosome of chickpea afects resistance to the root-lesion nematode Pratylenchus thornei.Crossref | GoogleScholarGoogle Scholar |
Kim HS, Sneller CH, Diers BW (1999) Evaluation of soybean cultivars for resistance to Sclerotinia stem rot in field environments. Crop Science 39, 64–68.
| Evaluation of soybean cultivars for resistance to Sclerotinia stem rot in field environments.Crossref | GoogleScholarGoogle Scholar |
Knights EJ, Hobson KB (2016) Chickpea: overview. In ‘Encyclopedia of food grains’. 2nd edn. (Eds C Wrigley, H Corke, K Seetharaman, J Faubion) pp. 316–323. (Academic Press: Oxford)
| Crossref |
Kottapalli P, Gaur PM, Katiyar SK, Crouch JH, Buhariwalla HK, Pande S, Gali KK (2009) Mapping and validation of QTLs for resistance to an Indian isolate of Ascochyta blight pathogen in chickpea. Euphytica 165, 79–88.
| Mapping and validation of QTLs for resistance to an Indian isolate of Ascochyta blight pathogen in chickpea.Crossref | GoogleScholarGoogle Scholar |
Lane D, Denton-Giles M, Derbyshire M, Kamphuis LG (2019) Abiotic conditions governing the myceliogenic germination of Sclerotinia sclerotiorum allowing the basal infection of Brassica napus. Australasian Plant Pathology 48, 85–91.
| Abiotic conditions governing the myceliogenic germination of Sclerotinia sclerotiorum allowing the basal infection of Brassica napus.Crossref | GoogleScholarGoogle Scholar |
Li H, Ye G, Wang J (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175, 361–374.
| A modified algorithm for the improvement of composite interval mapping.Crossref | GoogleScholarGoogle Scholar | 17110476PubMed |
Li S-B, Xie Z-Z, Hu C-G, Zhang J-Z (2016) A review of auxin response factors (ARFs) in plants. Frontiers in Plant Science 7, 47
| A review of auxin response factors (ARFs) in plants.Crossref | GoogleScholarGoogle Scholar | 26870066PubMed |
Li Y, Ruperao P, Batley J, Edwards D, Davidson J, Hobson K, Sutton T (2017) Genome analysis identified novel candidate genes for Ascochyta blight resistance in chickpea using whole genome re-sequencing data. Frontiers in Plant Science 8, 359
| Genome analysis identified novel candidate genes for Ascochyta blight resistance in chickpea using whole genome re-sequencing data.Crossref | GoogleScholarGoogle Scholar | 28367154PubMed |
Liang Y, Cason JM, Baring MR, Septiningsih EM (2021) Identification of QTLs associated with Sclerotinia blight resistance in peanut (Arachis hypogaea L.). Genetic Resources and Crop Evolution 68, 629–637.
| Identification of QTLs associated with Sclerotinia blight resistance in peanut (Arachis hypogaea L.).Crossref | GoogleScholarGoogle Scholar |
Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytologist 199, 639–649.
| APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs.Crossref | GoogleScholarGoogle Scholar |
Llorente F, Muskett P, Sánchez-Vallet A, López G, Ramos B, Sánchez-Rodríguez C, Jordá L, Parker J, Molina A (2008) Repression of the auxin response pathway increases arabidopsis susceptibility to necrotrophic fungi. Molecular Plant 1, 496–509.
| Repression of the auxin response pathway increases arabidopsis susceptibility to necrotrophic fungi.Crossref | GoogleScholarGoogle Scholar | 19825556PubMed |
McCaghey M, Willbur J, Ranjan A, Grau CR, Chapman S, Diers B, Groves C, Kabbage M, Smith DL (2017) Development and evaluation of Glycine max germplasm lines with quantitative resistance to Sclerotinia sclerotiorum. Frontiers in Plant Science 8, 1495
| Development and evaluation of Glycine max germplasm lines with quantitative resistance to Sclerotinia sclerotiorum.Crossref | GoogleScholarGoogle Scholar | 28912790PubMed |
Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. The Crop Journal 3, 269–283.
| QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations.Crossref | GoogleScholarGoogle Scholar |
Merga B, Haji J (2019) Economic importance of chickpea: production, value, and world trade. Cogent Food & Agriculture 5, 1615718
| Economic importance of chickpea: production, value, and world trade.Crossref | GoogleScholarGoogle Scholar |
Miklas PN (2007) Marker-assisted backcrossing QTL for partial resistance to Sclerotinia white mold in dry bean. Crop Science 47, 935–942.
| Marker-assisted backcrossing QTL for partial resistance to Sclerotinia white mold in dry bean.Crossref | GoogleScholarGoogle Scholar |
Mwape VW, Khentry Y, Newman TE, Denton-Giles M, Derbyshire MC, Chen K, Berger J, Kamphuis LG (2021a) Identification of sources of Sclerotinia sclerotiorum resistance in a collection of wild Cicer germplasm. Plant Disease 105, 2314–2324.
| Identification of sources of Sclerotinia sclerotiorum resistance in a collection of wild Cicer germplasm.Crossref | GoogleScholarGoogle Scholar | 33851865PubMed |
Mwape VW, Mobegi FM, Regmi R, Newman TE, Kamphuis LG, Derbyshire MC (2021b) Analysis of differentially expressed Sclerotinia sclerotiorum genes during the interaction with moderately resistant and highly susceptible chickpea lines. BMC Genomics 22, 333
| Analysis of differentially expressed Sclerotinia sclerotiorum genes during the interaction with moderately resistant and highly susceptible chickpea lines.Crossref | GoogleScholarGoogle Scholar | 33964897PubMed |
Perchepied L, Balagué C, Riou C, Claudel-Renard C, Rivière N, Grezes-Besset B, Roby D (2010) Nitric oxide participates in the complex interplay of defense-related signalling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 23, 846–860.
| Nitric oxide participates in the complex interplay of defense-related signalling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 20521948PubMed |
Pulse Australia (2020) APB Chickpea IDM strategies. Available at http://www.pulseaus.com.au/growing-pulses/bmp/chickpea/idm-strategies [Accessed 10 July 2020]
Qasim MU, Zhao Q, Shahid M, Samad RA, Ahmar S, Wu J, Fan C, Zhou Y (2020) Identification of QTLs containing resistance genes for Sclerotinia stem rot in Brassica napus using comparative transcriptomic studies. Frontiers in Plant Science 11, 776
| Identification of QTLs containing resistance genes for Sclerotinia stem rot in Brassica napus using comparative transcriptomic studies.Crossref | GoogleScholarGoogle Scholar | 32655594PubMed |
Royston JP (1982) An extension of Shapiro and Wilk’s W test for normality to large samples. Journal of the Royal Statistical Society Series C (Applied Statistics) 31, 115–124.
| An extension of Shapiro and Wilk’s W test for normality to large samples.Crossref | GoogleScholarGoogle Scholar |
Sabbavarapu MM, Sharma M, Chamarthi SK, Swapna N, Rathore A, Thudi M, Gaur PM, Pande S, Singh S, Kaur L, Varshney RK (2013) Molecular mapping of QTLs for resistance to Fusarium wilt (race 1) and Ascochyta blight in chickpea (Cicer arietinum L.). Euphytica 193, 121–133.
| Molecular mapping of QTLs for resistance to Fusarium wilt (race 1) and Ascochyta blight in chickpea (Cicer arietinum L.).Crossref | GoogleScholarGoogle Scholar |
Sagi MS, Deokar AA, Tar’an B (2017) Genetic analysis of NBS-LRR gene family in chickpea and their expression profiles in response to ascochyta blight infection. Frontiers in Plant Science 8, 838
| Genetic analysis of NBS-LRR gene family in chickpea and their expression profiles in response to ascochyta blight infection.Crossref | GoogleScholarGoogle Scholar | 28580004PubMed |
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52, 591–611.
| An analysis of variance test for normality (complete samples).Crossref | GoogleScholarGoogle Scholar |
Sharma M, Ghosh R (2016) An update on genetic resistance of chickpea to ascochyta blight. Agronomy 6, 18
| An update on genetic resistance of chickpea to ascochyta blight.Crossref | GoogleScholarGoogle Scholar |
Smith AB, Cullis BR, Thompson R (2005) The analysis of crop cultivar breeding and evaluation trials: an overview of current mixed model approaches. The Journal of Agricultural Science 143, 449–462.
| The analysis of crop cultivar breeding and evaluation trials: an overview of current mixed model approaches.Crossref | GoogleScholarGoogle Scholar |
Taylor J, Butler D (2017) R Package ASMap: efficient genetic linkage map construction and diagnosis. Journal of Statistical Software 79, 1–29.
| R Package ASMap: efficient genetic linkage map construction and diagnosis.Crossref | GoogleScholarGoogle Scholar |
Tewari SK, Pandey MP (1986) Genetics of resistance to ascochyta blight in chickpea (Cicer arietinum L.). Euphytica 35, 211–215.
| Genetics of resistance to ascochyta blight in chickpea (Cicer arietinum L.).Crossref | GoogleScholarGoogle Scholar |
Udupa SM, Sharma A, Sharma RP, Pai RA (1993) Narrow genetic variability in Cicer arietinum L. as revealed by RFLP analysis. Journal of Plant Biochemistry and Biotechnology 2, 83–86.
| Narrow genetic variability in Cicer arietinum L. as revealed by RFLP analysis.Crossref | GoogleScholarGoogle Scholar |
Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe AG, Cannon S, Baek J, Rosen BD, Tar’an B, Millan T, Zhang X, Ramsay LD, Iwata A, Wang Y, Nelson W, Farmer AD, Gaur PM, Soderlund C, Penmetsa RV, Xu C, Bharti AK, He W, Winter P, Zhao S, Hane JK, Carrasquilla-Garcia N, Condie JA, Upadhyaya HD, Luo M-C, Thudi M, Gowda CLL, Singh NP, Lichtenzveig J, Gali KK, Rubio J, Nadarajan N, Dolezel J, Bansal KC, Xu X, Edwards D, Zhang G, Kahl G, Gil J, Singh KB, Datta SK, Jackson SA, Wang J, Cook DR (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nature Biotechnology 31, 240–246.
| Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement.Crossref | GoogleScholarGoogle Scholar | 23354103PubMed |
Vuong TD, Hoffman DD, Diers BW, Miller JF, Steadman JR, Hartman GL (2004) Evaluation of soybean, dry bean, and sunflower for resistance to Sclerotinia sclerotiorum. Crop Science 44, 777–783.
| Evaluation of soybean, dry bean, and sunflower for resistance to Sclerotinia sclerotiorum.Crossref | GoogleScholarGoogle Scholar |
Wang Z, Tan X, Zhang Z, Gu S, Li G, Shi H (2012) Defense to Sclerotinia sclerotiorum in oilseed rape is associated with the sequential activations of salicylic acid signaling and jasmonic acid signaling. Plant Science 184, 75–82.
| Defense to Sclerotinia sclerotiorum in oilseed rape is associated with the sequential activations of salicylic acid signaling and jasmonic acid signaling.Crossref | GoogleScholarGoogle Scholar | 22284712PubMed |
Yamada T (1993) The role of auxin in plant-disease development. Annual Review of Phytopathology 31, 253–273.
| The role of auxin in plant-disease development.Crossref | GoogleScholarGoogle Scholar | 18643769PubMed |
Yang B, Jiang Y, Rahman MH, Deyholos MK, Kav NNV (2009) Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. BMC Plant Biology 9, 68
| Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments.Crossref | GoogleScholarGoogle Scholar | 19493335PubMed |
Yin X, Yi B, Chen W, Zhang W, Tu J, Fernando WGD, Fu T (2010) Mapping of QTLs detected in a Brassica napus DH population for resistance to Sclerotinia sclerotiorum in multiple environments. Euphytica 173, 25–35.
| Mapping of QTLs detected in a Brassica napus DH population for resistance to Sclerotinia sclerotiorum in multiple environments.Crossref | GoogleScholarGoogle Scholar |
Yue B, Radi SA, Vick BA, Cai X, Tang S, Knapp SJ, Gulya TJ, Miller JF, Hu J (2008) Identifying quantitative trait loci for resistance to Sclerotinia head rot in two USDA sunflower germplasms. Phytopathology 98, 926–931.
| Identifying quantitative trait loci for resistance to Sclerotinia head rot in two USDA sunflower germplasms.Crossref | GoogleScholarGoogle Scholar | 18943211PubMed |
Zhang L, Li H, Li Z, Wang J (2008) Interactions between markers can be caused by the dominance effect of quantitative trait loci. Genetics 180, 1177–1190.
| Interactions between markers can be caused by the dominance effect of quantitative trait loci.Crossref | GoogleScholarGoogle Scholar | 18780741PubMed |
Zhao W, Cheng X, Huang Z, Fan H, Wu H, Ling H-Q (2011) Tomato LeTHIC is an Fe-requiring HMP-P synthase involved in thiamine synthesis and regulated by multiple factors. Plant and Cell Physiology 52, 967–982.
| Tomato LeTHIC is an Fe-requiring HMP-P synthase involved in thiamine synthesis and regulated by multiple factors.Crossref | GoogleScholarGoogle Scholar | 21511719PubMed |
Zhou J, Sun A, Xing D (2013) Modulation of cellular redox status by thiamine-activated NADPH oxidase confers Arabidopsis resistance to Sclerotinia sclerotiorum. Journal of Experimental Botany 64, 3261–3272.
| Modulation of cellular redox status by thiamine-activated NADPH oxidase confers Arabidopsis resistance to Sclerotinia sclerotiorum.Crossref | GoogleScholarGoogle Scholar | 23814275PubMed |