Genetic determinants of lettuce resistance to drop caused by Sclerotinia minor identified through genome-wide association mapping frequently co-locate with loci regulating anthocyanin content.


Journal

TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik
ISSN: 1432-2242
Titre abrégé: Theor Appl Genet
Pays: Germany
ID NLM: 0145600

Informations de publication

Date de publication:
07 Aug 2023
Historique:
received: 12 12 2022
accepted: 12 07 2023
medline: 8 8 2023
pubmed: 7 8 2023
entrez: 7 8 2023
Statut: epublish

Résumé

GWAS identified 19 QTLs for resistance to Sclerotinia minor, 11 of them co-locating with red leaf color. Lower disease incidence was observed in red and dark red accessions. Lettuce (Lactuca sativa L.), one of the most economically important vegetables grown primarily in moderate climates around the world, is susceptible to many diseases including lettuce drop caused by the soilborne fungus Sclerotinia minor. Complete resistance to S. minor has not been identified in cultivated lettuce or its wild relatives. We conducted five experiments over 4 years with the diversity panel of almost 500 lettuce accessions to evaluate their response to the pathogen in an artificially infested field. The lowest disease incidence (DI) was observed in cultivars Eruption, Infantry, and Annapolis (median DI of 12.1-17.5%), while the highest DI was recorded for cultivars Reine des Glaces, Wayahead, and line FL. 43007 (median DI of 81.0-95.2%). Overall, significantly lower DI was observed in red and dark red accessions compared to those with a lower anthocyanin content. Genome-wide association mapping identified 19 QTLs for resistance to S. minor, 21 for the presence of red leaf color or its variations caused by the anthocyanin content, and one for the green color intensity. Eleven of the QTLs for disease resistance were located within 10 Mb of the loci associated with red color or anthocyanin content identified in this diversity panel. The frequent, non-random co-location of QTLs, together with the lower DI observed in red and dark red accessions suggests that lettuce interaction with S. minor may be partly influenced by anthocyanins. We have identified RLL2 and ANS, the genes of the anthocyanin biosynthesis pathway that co-locate with resistance QTLs, as candidates for functional studies to ascertain the involvement of anthocyanins in lettuce resistance against S. minor. Resistance QTLs closely linked with QTLs for anthocyanin content could be used to develop lettuce with a relatively high partial resistance and red color, while those not associated with anthocyanins could be used to develop partially resistant cultivars of green color.

Identifiants

pubmed: 37548768
doi: 10.1007/s00122-023-04421-y
pii: 10.1007/s00122-023-04421-y
doi:

Substances chimiques

Anthocyanins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

180

Informations de copyright

© 2023. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.

Références

Abawi GS, Robinson RW, Cobb AC, Shail JW (1980) Reaction of lettuce germ plasm to artificial inoculation with Sclerotinia minor under greenhouse conditions. Plant Dis 64:668–671
Almatwari AHA, Hassandokht M, Soltani F, Mirzadi Gohari A, Javan-Nikkhah M (2021) Temporal expression profiles of defense-related genes involved in Lactuca sativa-Sclerotinia sclerotiorum interactions. J Plant Pathol 103:61–69
An G, Qi Y, Zhang W, Gao H, Qian J, Larkin RM, Chen J, Kuang H (2022) LsNRL4 enhances photosynthesis and decreases leaf angles in lettuce. Plant Biotechnol J 20:1956–1967
pubmed: 35748307 pmcid: 9491448
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581
pubmed: 20674465
Dutton MV, Evans CS (1996) Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Can J Microbiol 42:881–895
Elia M, Piglionica V (1964) Osservazioni preliminari sulla resistenza di cultivars di lattuga ai “marciumi del colleto” da Sclerotinia spp. Phytopathol Mediterr 3:37–39
Farr DF, Bills GF, Chamuris GP, Rossman AY (1989) Fungi on plants and plant production in the United States. APS Press, St. Paul
Grube R, Ryder E (2004) Identification of lettuce (Lactuca sativa L.) germplasm with genetic resistance to drop caused by Sclerotinia minor. J Am Soc Hortic Sci 129:70–76
Gurdon C, Kozik A, Tao R, Poulev A, Armas I, Michelmore RW, Raskin I (2021) Isolating an active and inactive CACTA transposon from lettuce color mutants and characterizing their family. Plant Physiol 186:929–944
pubmed: 33768232 pmcid: 8195511
Hao J, Subbarao KV, Koike ST (2003a) Effects of broccoli rotation on lettuce drop caused by Sclerotinia minor and on the population density of sclerotia in soil. Plant Dis 87:159–166
pubmed: 30812921
Hao JJ, Subbarao KV, Duniway JM (2003b) Germination of Sclerotinia minor and S. sclerotiorum sclerotia under various soil moisture and temperature combinations. Phytopathology 93:443–450
pubmed: 18944359
Hayes RJ, Wu BM, Pryor BM, Chitrampalam P, Subbarao KV (2010) Assessment of resistance in lettuce (Lactuca sativa L.) to mycelial and ascospore infection by Sclerotinia minor Jagger and S. sclerotiorum (Lib.) de Bary. HortScience 45:333–341
Hayes RJ, Wu B, Subbarao KV (2011) A single recessive gene conferring short leaves in romaine × Latin type lettuce (Lactuca sativa L.) crosses, and its effect on plant morphology and resistance to lettuce drop caused by Sclerotinia minor Jagger. Plant Breed 130:388–393
Hubbard JC, Subbarao KV, Koike ST (1997) Development and significance of dicarboximide resistance in Sclerotinia minor isolates from commercial lettuce fields in California. Plant Dis 81:148–153
pubmed: 30870886
Imolehin ED, Grogan RG (1980) Factors affecting survival of sclerotia, and effects of inoculum density, relative position, and distance of sclerotia from the host on infection of lettuce by Sclerotinia minor. Phytopathology 70:1162–1167
Jaakola L (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci 18:477–483
pubmed: 23870661
Kwon S-J, Simko I, Hellier B, Mou B, Hu J (2013) Genome-wide association of 10 horticultural traits with expressed sequence tag-derived SNP markers in a collection of lettuce lines. Crop J 1:23–33
Li C, Yu W, Xu J, Lu X, Liu Y (2022) Anthocyanin biosynthesis induced by MYB transcription factors in plants. Int J Mol Sci 23:11701
pubmed: 36233003 pmcid: 9570290
Lin Y, Fan L, He J, Wang Z, Yin Y, Cheng Y, Li Z (2021) Anthocyanins contribute to fruit defense against postharvest green mold. Postharvest Biol Technol 181:111661
Liu X, Huang M, Fan B, Buckler ES, Zhang Z (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 12:e1005767
pubmed: 26828793 pmcid: 4734661
Liu R, Ding L-N, Li M, Cao W, Wang Y-K, Wang W-J, Yu Y-K, Wang Z, Zhu K-M, Tan X-L (2020) Characterization of a rapeseed anthocyanin-more mutant with enhanced resistance to Sclerotinia sclerotiorum. J Plant Growth Regul 39:703–716
Llorens E, Mateu M, González-Hernández AI, Agustí-Brisach C, García-Agustín P, Lapeña L, Vicedo B (2019) Extract of Mimosa tenuiflora and Quercus robur as potential eco-friendly management tool against Sclerotinia sclerotiorum in Lactuca sativa enhancing the natural plant defences. Eur J Plant Pathol 153:1105–1118
Long L, Zhao J-R, Xu F-C, Yang W-W, Liao P, Gao Y, Gao W, Song C-P (2018) Silencing of GbANS reduces cotton resistance to Verticillium dahliae through decreased ROS scavenging during the pathogen invasion process. Plant Cell Tissue Organ Cult 135:213–221
Mamo BE, Hayes RJ, Truco MJ, Puri KD, Michelmore RW, Subbarao KV, Simko I (2019) The genetics of resistance to lettuce drop (Sclerotinia spp.) in lettuce in a recombinant inbred line population from Reine des Glaces × Eruption. Theor Appl Genet 132:2439–2460
pubmed: 31165222
Mamo BE, Eriksen RL, Adhikari ND, Hayes RJ, Mou B, Simko I (2021) Epidemiological characterization of lettuce drop and biophysical features of the host identify soft stem as a susceptibility factor to Sclerotinia minor. PhytoFrontiers 1:182–204
Melzer MS, Smith EA, Boland GJ (1997) Index of plant hosts of Sclerotinia minor. Can J Plant Path 19:272–280
Naing AH, Kim CK (2021) Abiotic stress-induced anthocyanins in plants: their role in tolerance to abiotic stresses. Physiol Plant 172:1711–1723
pubmed: 33605458
Ott A, Liu S, Schnable JC, Yeh C-TE, Wang K-S, Schnable PS (2017) tGBS® genotyping-by-sequencing enables reliable genotyping of heterozygous loci. Nucleic Acids Res 45:e178
pubmed: 29036322 pmcid: 5716196
Pink H, Talbot A, Graceson A, Graham J, Higgins G, Taylor A, Jackson AC, Truco M, Michelmore R, Yao C, Gawthrop F, Pink D, Hand P, Clarkson JP, Denby K (2022) Identification of genetic loci in lettuce mediating quantitative resistance to fungal pathogens. Theor Appl Genet 135:2481–2500
pubmed: 35674778 pmcid: 9271113
Pojer E, Mattivi F, Johnson D, Stockley CS (2013) The case for anthocyanin consumption to promote human health: a review. Compr Rev Food Sci Food Saf 12:483–508
pubmed: 33412667
Reyes-Chin-Wo S, Wang Z, Yang X, Kozik A, Arikit S, Song C, Xia L, Froenicke L, Lavelle DO, Truco M-J, Xia R, Zhu S, Xu C, Xu H, Xu X, Cox K, Korf I, Mayers BC, Michelmore RW (2017) Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nat Commun 8:14953
pubmed: 28401891 pmcid: 5394340
Simko I (2004) One potato, two potato: haplotype association mapping in autotetraploids. Trends Plant Sci 9:441–448
pubmed: 15337494
Simko I (2019) Genetic variation and relationship among content of vitamins, pigments, and sugars in baby leaf lettuce. Food Sci Nutr 7:3317–3326
pubmed: 31660145 pmcid: 6804913
Simko I (2020a) Genetic variation in response to N, P, or K deprivation in baby leaf lettuce. Horticulturae 6:15
Simko I (2020b) Predictive modeling of a leaf conceptual midpoint quasi-color (CMQ) using an artificial neural network. Sensors 20:3938
pubmed: 32679776 pmcid: 7412459
Simko I (2023) Dataset on the single nucleotide variation in diversity panel of 500 lettuce accessions genotyped with tunable genotyping-by-sequencing (tGBS) method. Data Brief 49:109419
pubmed: 37538955 pmcid: 10393593
Simko I, Linacre JM (2010) Combining partially ranked data in plant breeding and biology: II. Analysis with Rasch model. Commun Biometry Crop Sci 5:56–65
Simko I, Pechenick DA (2010) Combining partially ranked data in plant breeding and biology: I. Rank aggregating methods. Commun Biometry Crop Sci 5:41–55
Simko I, Piepho HP (2011) Combining phenotypic data from ordinal rating scales in multiple plant experiments. Trends Plant Sci 16:235–237
pubmed: 21367649
Simko I, Atallah AJ, Ochoa OE, Antonise R, Galeano CH, Truco MJ, Michelmore RW (2013) Identification of QTLs conferring resistance to downy mildew in legacy cultivars of lettuce. Sci Rep 3:2875
pubmed: 24096732 pmcid: 3791445
Simko I, Hayes RJ, Mou B, McCreight JD (2014) Lettuce and Spinach. In: Smith S, Diers B, Specht J, Carver B (eds) Yield gains in major US field crops. American Society of Agronomy, Inc., Crop Science Society of America, Inc., and Soil Science Society of America, Inc., pp 53–86
Simko I, Hayes RJ, Furbank RT (2016) Non-destructive phenotyping of lettuce plants in early stages of development with optical sensors. Front Plant Sci 7:1985
pubmed: 28083011 pmcid: 5187177
Simko I, Sandoya G, Orozco J, Sthapit Kandel J, Zhao R, Subarao KV, Hayes RJ (2020) Notice of release of romaine lettuce germplasm with resistance to lettuce drop disease P.0022.20: https://calgreens.org/wp-content/uploads/2022/03/Romaine-Lettuce-with-improved-resistance-to-Sclerotina-2020-1.pdf
Simko I, Jia M, Venkatesh J, Kang B-C, Weng Y, Barcaccia G, Lanteri S, Bhattarai G, Foolad MR (2021) Genomics and marker-assisted improvement of vegetable crops. Crit Rev Plant Sci 40:303–365
Simko I, Peng H, Sthapit Kandel J, Zhao R (2022a) Genome-wide association mapping reveals genomic regions frequently associated with lettuce field resistance to downy mildew. Theor Appl Genet 135:2009–2024
pubmed: 35419653
Simko I, Puri KD, Dhar N, Peng H, Subbarao KV (2022b) Mapping QTLs for lettuce resistance to Verticillium dahliae race 3, plant development and leaf color using an ultra-high-density bin map constructed from F
Simko I, Hasegawa DK, Peng H, Zhao R (2023) Genetic and physiological determinants of lettuce partial resistance to Impatiens necrotic spot virus. Front Plant Sci 14:1163683
pubmed: 37360711 pmcid: 10285314
Singh M, Avtar R, Lakra N, Pal A, Singh VK, Punia R, Kumar N, Bishnoi M, Kumari N, Khedwal RS (2022) Early oxidative burst and anthocyanin-mediated antioxidant defense mechanism impart resistance against Sclerotinia sclerotiorum in Indian mustard. Physiol Mol Plant Pathol 120:101847
Sthapit Kandel J, Peng H, Hayes RJ, Mou B, Simko I (2020) Genome-wide association mapping reveals loci for shelf life and developmental rate of lettuce. Theor Appl Genet 133:1947–1966
pubmed: 32123958
Su W, Tao R, Liu W, Yu C, Yue Z, He S, Lavelle D, Zhang W, Zhang L, An G, Zhang Y, Hu Q, Larkin RM, Michelmore RW, Kuang H, Chen J (2019) Characterization of four polymorphic genes controlling red leaf colour in lettuce that have undergone disruptive selection since domestication. Plant Biotechnol J 18:479–490
pubmed: 31325407 pmcid: 6953203
Subbarao KV (1998) Progress toward integrated management of lettuce drop. Plant Dis 82:1068–1078
pubmed: 30856764
Subbarao KV, Koike ST, Hubbard JC (1996) Effects of deep plowing on the distribution and density of Sclerotinia minor sclerotia and lettuce drop incidence. Plant Dis 80:28–33
Wada KC, Inagaki N, Sakai H, Yamashita H, Nakai Y, Fujimoto Z, Yonemaru J-i, Itoh H (2022) Genetic effects of Red Lettuce Leaf genes on red coloration in leaf lettuce under artificial lighting conditions. Plant-Environ Interact 3:179–192
pubmed: 37283610 pmcid: 10168059
Wang Q, Tian F, Pan Y, Buckler ES, Zhang Z (2014) A SUPER powerful method for genome wide association study. PLoS ONE 9:e107684
pubmed: 25247812 pmcid: 4172578
Wei T, van Treuren R, Liu X, Zhang Z, Chen J, Liu Y, Dong S, Sun P, Yang T, Lan T, Wang X, Xiong Z, Liu Y, Wei J, Lu H, Han S, Chen JC, Ni X, Wang J, Yang H, Xu X, Kuang H, van Hintum T, Liu X, Liu H (2021) Whole-genome resequencing of 445 Lactuca accessions reveals the domestication history of cultivated lettuce. Nat Genet 53:752–760
pubmed: 33846635
Wolfinger R, Federer WT, Cordero-Brana O (1997) Recovering information in augmented designs, using SAS PROC GLM and PROC MIXED. Agron J 89:856–859
Wu BM, Subbarao KV (2003) Effects of irrigation and tillage on temporal and spatial dynamics of Sclerotinia minor sclerotia and lettuce drop incidence. Phytopathology 93:1572–1580
pubmed: 18943622
Wu BM, Subbarao KV (2017) Lettuce drop. In: Subbarao KV, Davis RM, Gilbertson RL, Raid RN (eds) Compendium of lettuce diseases and pests, Second edition. APS Press, St. Paul, pp 222–244
Wu BM, Subbarao KV, Liu YB (2008) Comparative survival of sclerotia of Sclerotinia minor and S. sclerotiorum. Phytopathology 98:659–665
pubmed: 18944289
Wu J, Zhao Q, Liu S, Shahid M, Lan L, Cai G, Zhang C, Fan C, Wang Y, Zhou Y (2016) Genome-wide association study identifies new loci for resistance to Sclerotinia stem rot in Brassica napus. Front Plant Sci 7:1418
pubmed: 27703464 pmcid: 5028409
Zhang Y, Butelli E, De Stefano R, Schoonbeek H-j, Magusin A, Pagliarani C, Wellner N, Hill L, Orzaez D, Granell A (2013) Anthocyanins double the shelf life of tomatoes by delaying overripening and reducing susceptibility to gray mold. Curr Biol 23:1094–1100
pubmed: 23707429 pmcid: 3688073
Zhang L, Su W, Tao R, Zhang W, Chen J, Wu P, Yan C, Jia Y, Larkin RM, Lavelle D, Truco M-J, Reyes-Chin-Wo S, Michelmore RW, Kuang H (2017) RNA sequencing provides insights into the evolution of lettuce and the regulation of flavonoid biosynthesis. Nat Commun 8:2264
pubmed: 29273740 pmcid: 5741661
Zhang L, Qian J, Han Y, Jia Y, Kuang H, Chen J (2022) Alternative splicing triggered by the insertion of a CACTA transposon attenuates LsGLK and leads to the development of pale-green leaves in lettuce. Plant J 109:182–195
pubmed: 34724596
Zhao X, Han Y, Li Y, Liu D, Sun M, Zhao Y, Lv C, Li D, Yang Z, Huang L, Weili T, Qiu L, Zheng H, Li W (2015) Loci and candidate gene identification for resistance to Sclerotinia sclerotiorum in soybean (Glycine max L. Merr.) via association and linkage maps. Plant J 82:245–255
pubmed: 25736370
Zhu H, Li X, Zhai W, Liu Y, Gao Q, Liu J, Ren L, Chen H, Zhu Y (2017) Effects of low light on photosynthetic properties, antioxidant enzyme activity, and anthocyanin accumulation in purple pak-choi (Brassica campestris ssp. Chinensis Makino). PLoS ONE 12:e0179305
pubmed: 28609452 pmcid: 5469474

Auteurs

Ivan Simko (I)

Crop Improvement and Protection Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Salinas, CA, 93905, USA. ivan.simko@usda.gov.

Jinita Sthapit Kandel (J)

Edward T. Schafer Agricultural Research Center, U.S. Department of Agriculture, Agricultural Research Service, Fargo, ND, 58102, USA.

Hui Peng (H)

Everglades Research and Education Center, Horticultural Sciences Department, University of Florida, Belle Glade, FL, 33430, USA.

Rebecca Zhao (R)

Crop Improvement and Protection Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Salinas, CA, 93905, USA.

Krishna V Subbarao (KV)

Department of Plant Pathology, University of California, Davis, c/o U.S., Agricultural Research Station, Salinas, CA, 93905, USA. kvsubbarao@ucdavis.edu.

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