The MLO1 powdery mildew susceptibility gene in Lathyrus species: The power of high-density linkage maps in comparative mapping and synteny analysis.
Journal
The plant genome
ISSN: 1940-3372
Titre abrégé: Plant Genome
Pays: United States
ID NLM: 101273919
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
25
11
2020
accepted:
31
01
2020
pubmed:
8
5
2021
medline:
24
9
2021
entrez:
7
5
2021
Statut:
ppublish
Résumé
Powdery mildews are major diseases for a range of crops. The loss of function of specific Mildew Locus O (MLO) genes has long been associated with pre-haustorial plant resistance to powdery mildew and has proven to be durable in several species. Erysiphe pisi is the major causal agent of powdery mildew in pea (Pisum sativum L.) and in the closely related Lathyrus sativus L. and Lathyrus cicera L. PsMLO1 has been extensively studied in pea. However, no MLO gene family members have been isolated and characterized in Lathyrus species so far. In this study, MLO1 genes were isolated and characterized in L. sativus and L. cicera genotypes with varied levels of partial resistance against powdery mildew. Phylogenetic analyses confirmed that Lathyrus MLO1 belongs to Clade V, like all dicot MLO proteins associated with powdery mildew susceptibility. A L. sativus recombinant inbred line population (RIL) was genotyped by sequencing to develop a high-density L. sativus genetic linkage map. DNA sequence polymorphisms between the analyzed genotypes allowed the location of MLO1 in the newly developed L. sativus RIL genetic linkage map. Subsequent comparative mapping between L. sativus and L. cicera genetic maps and P. sativum, Lens culinaris Medik., and Medicago truncatula Gaertn. reference genomes revealed important aspects of the conservation of the MLO1 locus position and of the overall chromosomal rearrangements occurring during legume evolution, with relevance to legume disease resistance breeding programs.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e20090Informations de copyright
© 2021 The Authors. The Plant Genome published by Wiley Periodicals LLC on behalf of Crop Science Society of America.
Références
Acevedo-Garcia, J., Kusch, S., & Panstruga, R. (2014). Magical mystery tour : MLO proteins in plant immunity and beyond. New Phytologist, 204, 273-281. https://doi.org/10.1111/nph.12889
Acevedo-Garcia, J., Spencer, D., Thieron, H., Reinstädler, A., Hammond-Kosack, K., Phillips, A. L., & Panstruga, R. (2017). mlo-based powdery mildew resistance in hexaploid bread wheat generated by a non-transgenic TILLING approach. Plant Biotechnology Journal, 15, 367-378. https://doi.org/10.1111/pbi.12631
Almagro Armenteros, J. J., Tsirigos, K. D., Sønderby, C. K., Petersen, T. N., Winther, O., Brunak, S., … Henrik, N. (2019). SignalP 5.0 improves signal peptide predictions using deep neural networks. Nature Biotechnology, 37, 420-423. https://doi.org/10.1038/s41587-019-0036-z
Almeida, N. F., Leitão, S. T., Krezdorn, N., Rotter, B., Winter, P., Rubiales, D., & Vaz Patto, M. C. (2014). Allelic diversity in the transcriptomes of contrasting rust-infected genotypes of Lathyrus sativus, a lasting resource for smart breeding. BMC Plant Biology, 14, 376. https://doi.org/10.1186/s12870-014-0376-2
Bai, Y., Pavan, S., Zheng, Z., Zappel, N. F., Reinstädler, A., Lotti, C., … Panstruga, R. (2008). Naturally occurring broad-spectrum powdery mildew resistance in a Central American tomato accession is caused by loss of Mlo function. Molecular Plant-Microbe Interactions, 21, 30-39. https://doi.org/10.1094/MPMI-21-1-0030
Barilli, E., Rubiales, D., Gjetting, T., & Lyngkjaer, M. F. (2014). Differential gene transcript accumulation in peas in response to powdery mildew (Erysiphe pisi) attack. Euphytica, 198, 13-28. https://doi.org/10.1007/s10681-014-1062-z
Bayer, M., Milne, I., Stephen, G., Shaw, P., Cardle, L., Wright, F., & Marshall, D. (2011). Comparative visualization of genetic and physical maps with strudel. Bioinformatics, 27, 1307-1308. https://doi.org/10.1093/bioinformatics/btr111
Chauhan, H., Boni, R., Bucher, R., Kuhn, B., Buchmann, G., Sucher, … Keller, B. (2015). The wheat resistance gene Lr34 results in the constitutive induction of multiple defense pathways in transgenic barley. The Plant Journal, 84, 202-215. https://doi.org/10.1111/tpj.13001
Chou, K. C., Shen, H.-B. (2010). Plant-mPLoc: A top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS One, 5, e11335. https://doi.org/10.1371/journal.pone.0011335
Chowdhury, M. A., & Slinkard, A. E. (1999). Linkage of random amplified polymorphic DNA, isozyme and morphological markers in grasspea (Lathyrus sativus). Journal of Agricultural Science, 133, 389-395. https://doi.org/10.1017/S0021859699007108
Deshmukh, R., Singh, V. K., & Singh, B. D. (2014). Comparative phylogenetic analysis of genome-wide Mlo gene family members from Glycine max and Arabidopsis thaliana. Molecular Genetics and Genomics, 289, 345-359. https://doi.org/10.1007/s00438-014-0811-y
Dobson, L., Reményi, I., & Tusnády, G. E. (2015). CCTOP: A Consensus Constrained TOPology prediction web server. Nucleic Acids Research, 43, W408-W412. https://doi.org/10.1093/nar/gkv451
Elliott, C., Müller, J., Miklis, M., Bhat, R. A., Schulze-Lefert, P., & Panstruga, R. (2005). Conserved extracellular cysteine residues and cytoplasmic loop-loop interplay are required for functionality of the heptahelical MLO protein. Biochemical Journal, 385, 243-254. https://doi.org/10.1042/BJ20040993
Emmrich, P. M. F., Sarkar, A., Njaci, I., Kaithakottil, G. G., Ellis, N., Moore, C., … Wang, T. L. (2020). A draft genome of grass pea (Lathyrus sativus), a resilient diploid legume. bioRxiv, 058164. https://doi.org/10.1101/2020.04.24.058164
Fondevilla, S., Carver, T. L. W., Moreno, M. T., & Rubiales, D. (2006). Macroscopic and histological characterisation of genes er1 and er2 for powdery mildew resistance in pea. European Journal of Plant Pathology, 115, 309-321. https://doi.org/10.1007/s10658-006-9015-6
Fondevilla, S., Cubero, J. I., & Rubiales, D. (2011). Confirmation that the Er3 gene, conferring resistance to Erysiphe pisi in pea, is a different gene from er1 and er2 genes. Plant Breeding, 130, 281-282. https://doi.org/10.1111/j.1439-0523.2010.01769.x
Fondevilla, S., & Rubiales, D. (2012). Powdery mildew control in pea. A review. Agronomy for Sustainable Development, 32, 401-409. https://doi.org/10.1007/s13593-011-0033-1
Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., & Bairoch, A. (2005). Protein identification and analysis tools on the ExPASy server. In J.M. Walker (Ed.), The proteomics protocols handbook (pp. 571-607). Totowa, NJ: Humana Press. https://doi.org/10.1385/1-59259-890-0:571
Glawe, D. A. (2008). The powdery mildews: A review of the world's most familiar (yet poorly known) plant pathogens. Annual Review of Phytopathology, 46, 27-51. https://doi.org/10.1146/annurev.phyto.46.081407.104740.
Hu, B., Jin, J., Guo, A. Y., Zhang, H., Luo, J., & Gao, G. (2015). GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics, 31, 1296-1297. https://doi.org/10.1093/bioinformatics/btu817
Humphry, M., Reinstädler, A., Ivanov, S., Bisseling, T., & Panstruga, R. (2011). Durable broad-spectrum powdery mildew resistance in pea er1 plants is conferred by natural loss-of-function mutations in PsMLO1. Molecular Plant Pathology, 12, 866-878. https://doi.org/10.1111/j.1364-3703.2011.00718.x
Iglesias-García, R., Rubiales, D., & Fondevilla, S. (2015). Penetration resistance to Erysiphe pisi in pea mediated by er1 gene is associated with protein cross-linking but not with callose apposition or hypersensitive response. Euphytica, 201, 381-387. https://doi.org/10.1007/s10681-014-1221-2
Jørgensen, I. H. (1992). Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica, 63, 141-152. https://doi.org/10.1007/BF00023919
Koonin, E. V., & Galperin, M. Y. (2003). Sequence - evolution - function: Computational approaches in comparative genomics. Boston, MA: Kluwer Academic.
Kreplak, J., Madoui, M.-A., Cápal, P., Novák, P., Labadie, K., Aubert, G., … Burstin, J. (2019). A reference genome for pea provides insight into legume genome evolution. Nature Genetics, 51, 1411-1422. https://doi.org/10.1038/s41588-019-0480-1
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolotion, 35, 1547-1549. https://doi.org/10.1093/molbev/msy096
Lambein, F., Travella, S., Kuo, Y.-H., Van Montagu, M., & Heijde, M. (2019). Grass pea (Lathyrus sativus L.): Orphan crop, nutraceutical or just plain food? Planta, 250, 821-838. https://doi.org/10.1007/s00425-018-03084-0
Lee, J., Feng, J., Campbell, K. B., Scheffler, B. E., Garrett, W. M., Thibivilliers, S., … Cooper, B. (2009). Quantitative proteomic analysis of bean plants infected by a virulent and avirulent obligate rust fungus. Molecular & Cellular Proteomics, 8, 19-31. https://doi.org/10.1074/mcp.M800156-MCP200
Liu, W., Xie, Y., Ma, J., Luo, X., Nie, P., Zuo, Z., … Ren, J. (2015). IBS: An illustrator for the presentation and visualization of biological sequences. Bioinformatics, 31, 3359-3361. https://doi.org/10.1093/bioinformatics/btv362
Lyngkjaer, M. F., Newton, A. C., Atzema, J. L., & Baker, S. J. (2000). The barley mlo-gene: An important powdery mildew resistance source. Agronomie, 20, 745-756. https://doi.org/10.1051/agro:2000173
Martins, D., Araújo, S. S., Rubiales, D., & Vaz Patto, M. C. (2020). Legume crops and biotrophic pathogen interactions: A continuous cross-talk of a multilayered array of defense mechanisms. Plants, 9, 1460, https://doi.org/10.3390/plants9111460
Marquez, Y., Brown, J. W. S., Simpson, C., Barta, A., & Kalyna, M. (2012). Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Research, 22, 1184-1195. https://doi.org/10.1101/gr.134106.111
Niks, R. E., Qi, X., & Marcel, T. C. (2015). Quantitative resistance to biotrophic filamentous plant pathogens: Concepts, misconceptions, and mechanisms. Annual Review of Phytopathology, 53, 445-470. https://doi.org/10.1146/annurev-phyto-080614-115928
Niks, R. E., & Rubiales, D. (2002). Potentially durable resistance mechanisms in plants to specialised fungal pathogens. Euphytica, 124, 201-216. https://doi.org/10.1023/A:1015634617334
Pavan, S., Jacobsen, E., Visser, R. G. F., & Bai, Y. (2010). Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Molecular Breeding, 25, 1-12. https://doi.org/10.1007/s11032-009-9323-6
Pavan, S., Schiavulli, A., Appiano, M., Marcotrigiano, A. R., Cillo, F., Visser, R. G. F., … Ricciardi, L. (2011). Pea powdery mildew er1 resistance is associated to loss-of-function mutations at a MLO homologous locus. Theoretical and Applied Genetics, 123, 1425-1431. https://doi.org/10.1007/s00122-011-1677-6
Polanco, C., Sáenz de Miera, L. E., Bett, K., & Pérez de la Vega, M. (2018). A genome-wide identification and comparative analysis of the lentil MLO genes. PLoS One, 13, e0194945. https://doi.org/10.1371/journal.pone.0194945
Prats, E., Llamas, M. J., & Rubiales, D. (2007). Characterization of resistance mechanisms to Erysiphe pisi in Medicago truncatula. Phytopathology, 97, 1049-1053. https://doi.org/10.1094/PHYTO-97-9-1049
Reinstädler, A., Müller, J., Czembor, J. H., Piffanelli, P., & Panstruga, R. (2010). Novel induced mlo mutant alleles in combination with site-directed mutagenesis reveal functionally important domains in the heptahelical barley Mlo protein. BMC Plant Biology, 10, 31. https://doi.org/10.1186/1471-2229-10-31
Rispail, N., & Rubiales, D. (2016). Genome-wide identification and comparison of legume MLO gene family. Scientific Reports, 6, 1-12. https://doi.org/10.1038/srep32673
Santos, C., Almeida, N. F., Alves, M. L., Horres, R., Krezdorn, N., Leitão, S. T., … Vaz Patto, M. C. (2018). First genetic linkage map of Lathyrus cicera based on RNA sequencing-derived markers: Key tool for genetic mapping of disease resistance. Horticulture Research, 5, 1-14. https://doi.org/10.1038/s41438-018-0047-9
Santos, C., Martins, D., Rubiales, D., & Vaz Patto, M. C. (2020). Partial resistance against Erysiphe pisi and E. trifolii under different genetic control in Lathyrus cicera: Outcomes from a linkage mapping approach. Plant Disease, 5, 45. https://doi.org/10.1038/s41438-018-0047-9
Skiba, B., Ford, R., & Pang, E. C. K. (2004). Construction of a linkage map based on a Lathyrus sativus backcross population and preliminary investigation of QTLs associated with resistance to ascochyta blight. Theoretical and Applied Genetics, 109, 1726-1735. https://doi.org/10.1007/s00122-004-1812-8
Solovyev, V., Kosarev, P., Seledsov, I., & Vorobyev, D. (2006). Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biology, 7, S10. https://doi.org/10.1186/gb-2006-7-s1-s10
Tang, H., Krishnakumar, V., Bidwell, S., Rosen, B., Chan, A., Zhou, S., … Town, C. D. (2014). An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genomics, 15, 312. https://doi.org/10.1186/1471-2164-15-312
Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R., & Leunissen, J. A. M. (2007). Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research, 35, W71-W7. https://doi.org/10.1093/nar/gkm306
Van Ooijen, J. W. (2006). JoinMap 4, Software for the calculation of genetic linkage maps in experimental populations. Wageningen, Netherlands: Kyazma B.V.
Vaz Patto, M. C., Amarowicz, R., Aryee, A. N. A., Boye, J. I., Chung, H.-J., Martín-Cabrejas, M. A., & Domoney, C. (2015). Achievements and challenges in improving the nutritional quality of food legumes. Critical Reviews in Plant Sciences, 34, 105-143. https://doi.org/10.1080/07352689.2014.897907
Vaz Patto, M. C., Fernández-Aparicio, M., Moral, A., & Rubiales, D. (2006). Characterization of resistance to powdery mildew (Erysiphe pisi) in a germplasm collection of Lathyrus sativus. Plant Breeding, 125, 308-310. https://doi.org/10.1111/j.1439-0523.2006.01220.x
Vaz Patto, M. C., Fernández-Aparicio, M., Moral, A., & Rubiales, D. (2007). Resistance reaction to powdery mildew (Erysiphe pisi) in a germplasm collection of Lathyrus cicera from Iberian origin. Genetic Resources and Crop Evolution, 54, 1517-1521. https://doi.org/10.1007/s10722-006-9142-0
Vaz Patto, M. C., Fernández-Aparicio, M., Moral, A., & Rubiales, D. (2009). Pre and posthaustorial resistance to rusts in Lathyrus cicera L. Euphytica, 165, 27-34. https://doi.org/10.1007/s10681-008-9737-y
Vaz Patto, M. C., & Rubiales, D. (2009). Identification and characterization of partial resistance to rust in a germplasm collection of Lathyrus sativus L. Plant Breeding, 128, 495-500. https://doi.org/10.1111/j.1439-0523.2008.01601.x
Voorrips, R. E. (2002). MapChart: Software for the graphical presentation of linkage maps and QTLs. Journal of Heredity, 93, 77-78. https://doi.org/10.1093/JHERED/93.1.77.
Ye, S., Dhilon, S., Ke, X., Collins, A. R., & Day, I. N. M. (2001). An efficient procedure for genotyping single nucleotide polymorphisms. Nucleic Acids Research, 29, e88. https://doi.org/10.1093/nar/29.17.e88