Genetic mapping and survey of powdery mildew resistance in the wild Central Asian ancestor of cultivated grapevines in Central Asia

Summaira Riaz , Cristina M. Menéndez , Alan Tenscher , Daniel Pap , M. Andrew Walker

Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) : 104

PDF (1200KB)
Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) :104 DOI: 10.1038/s41438-020-0335-z
Article
research-article
Genetic mapping and survey of powdery mildew resistance in the wild Central Asian ancestor of cultivated grapevines in Central Asia
Author information +
History +
PDF (1200KB)

Abstract

Cultivated grapevines (Vitis vinifera) lack resistance to powdery mildew (PM) with few exceptions. Resistance to this pathogen within V. vinifera has been reported in earlier studies and identified as the Ren1 locus in two Central Asian table grape accessions. Other PM-resistant cultivated varieties and accessions of the wild ancestor V. vinifera subsp. sylvestris were soon identified raising questions regarding the origin of the resistance. In this study, F1 breeding populations were developed with a PM susceptible V. vinifera subsp. vinifera breeding line and a PM-resistant subsp. sylvestris accession. Genotyping was carried out with five Ren1 locus linked SSR markers. A PM resistance locus explaining up to 96% of the phenotypic variation was identified in the same genomic position, where the Ren1 locus was previously reported. New SSR marker alleles linked with the resistance locus were identified. We report results of PM resistance in multiple accessions of subsp. sylvestris collected as seed lots or cuttings from five countries in the Caucasus and Central Asia. A total of 20 females from 11 seed lots and 19 males from nine seed lots collected from Georgia, Armenia, and Azerbaijan were resistant to PM. Three male and one female plant collected as cuttings from Afghanistan and Iran were also resistant to PM. Allelic analysis of markers linked with the Ren1 locus in conjunction with disease evaluation data found a high diversity of allelic haplotypes, which are only possible via recombination events occurring over a long time period. Sequence analysis of two alleles of the SSR marker that cosegregates with the resistance found SNPs that were present in the wild progenitor and in cultivated forms. Variable levels of PM resistance among the tested accessions were also observed. These lines of evidence suggest that the powdery mildew fungus may have been present in Asia for a longer time than currently thought, giving the wild progenitor V. vinifera subsp. sylvestris time to coevolve with and develop resistance to this pathogen.

Cite this article

Download citation ▾
Summaira Riaz, Cristina M. Menéndez, Alan Tenscher, Daniel Pap, M. Andrew Walker. Genetic mapping and survey of powdery mildew resistance in the wild Central Asian ancestor of cultivated grapevines in Central Asia. Horticulture Research, 2020, 7 (1) : 104 DOI:10.1038/s41438-020-0335-z

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Myles, S. et al. Genetic structure and domestication history of the grape. Proc. Natl Acad. Sci. USA 108, 3530-3535 (2011).

[2]

Wan, Y. et al. The eco-geographic distribution of wild grape germplasm in China. Vitis 47, 77-80 (2008).

[3]

Wan, Y. et al. A phylogenetic analysis of the grape genus (Vitis L.) reveals broad reticulation and concurrent diversification during Neogene and Quaternary climate change. BMC Evol. Biol. 13, 141 (2013).

[4]

This, P., Lacombe, T. & Thomas, M. R. Historical origins and genetic diversity of wine grapes. Trends Genet. 22, 511-519 (2006).

[5]

Grassi, F. et al. Phylogeographical structure and conservation genetics of wild grapevine. Conserv. Genet. 7, 837-845 (2006).

[6]

Negrul, A. M. Evolution of cultivated forms of grapes. C. R. Acad. Sci. URSS 18, 585-588 (1938).

[7]

Riaz, S. et al. Analysis of the genetic diversity and structure of cultivated and wild grapevine (Vitis vinifera L.) accessions around the Mediterranean basin and Central Asia regions. BMC Plant Biol. 18, 137 (2018).

[8]

Adler, D. S. & Tushabramishvili, N. in Settlement Dynamics of the Middle Paleolithic and Middle Stone Age. Vol. 2 (ed. Conard, N. J.) Ch. 5 (Kerns Verlag Tübingen, 2004).

[9]

McGovern, P. E. (ed.) Ancient Wine: The Search for the Origins of Viniculture 1st edn. (Princeton Univ. Press, 2003)

[10]

Hoffmann, S. et al. Resistance to Erysiphe necator in the grapevine ‘Kishmish vatkana’ is controlled by a single locus through restriction of hyphal growth. Theor. Appl. Genet. 116, 427-438 (2008).

[11]

Riaz, S. et al. Identification of mildew resistance in wild and cultivated Central Asian grape germplasm. BMC Plant Biol. 13, 149 (2013).

[12]

Large, E. C. (ed.) The Advance of the Fungi. (Henry Holt and Co, New York, 1940)

[13]

Weltzien, H. C. in The Powdery Mildews. (ed. Spencer, D. M.) (Academic Press, 1978).

[14]

Lutz, H. F. (ed.) Viticulture and Brewing in the Ancient Orient. (J.C. Hinrichs’sche Buchhandlung, 1922).

[15]

Vavilov, N. I. Cemtry proiskhozhdenia kulturnikh rastenii (The centers of origin for cultivated plants). Proc. Appl. Bot. Genet. Breed. 16, 133-137 (1926).

[16]

Negrul, A. M. in The Ampelography of the USSR. Vol. 1 (eds. Baranov, A. et al. ) pp. 159-216. (Pischepromizdat, 1946).

[17]

Wan, Y., Schwaniniger, H., He, P. & Wang, Y. Comparison of resistance to powdery mildew and downy mildew in Chinese wild grapes. Vitis 46, 132-136 (2007).

[18]

Riaz, S., Tenscher, A. C., Ramming, D. W. & Walker, M. A. Using a limited mapping strategy to identify major QTLs for resistance to grapevine powdery mildew (Erysiphe necator) and their use in marker-assisted breeding. Theor. Appl. Genet. 122, 1059-1073 (2011).

[19]

Ramming, D. W. et al. Identification of race-specific resistance in North American Vitis spp. limiting Erysiphe necator hyphal growth. Phytopathology 102, 83-93 (2012).

[20]

Pap, D. et al. Identification of two novel powdery mildew resistance loci, Ren6 and Ren7, from the wild Chinese grape species Vitis piasezkii. BMC Plant Biol. 16, 170 (2016).

[21]

Coleman, C. et al. The powdery mildew resistance gene REN1 co-segregates with an NBS-LRR gene cluster in two Central Asian grapevines. BMC Genet. 10, 89 (2009).

[22]

Burgarella, C. et al. Adaptive introgression: an untapped evolutionary mechanism for crop adaptation. Front Plant Sci. 10, 4 (2019).

[23]

Barrett, L. G., Kniskern, J. M., Bodenhausen, N., Zhang, W. & Bergelson, J. Continua of specificity and virulence in plant host-pathogen interactions: causes and consequences. N. Phytol. 183, 513-529 (2009).

[24]

Vekemans, X. What’s good for you may be good for me: evidence for adaptive introgression of multiple traits in wild sunflower. N. Phytol. 187, 7-9 (2010).

[25]

Whitney, K. D., Randell, R. A. & Rieseberg, L. H. Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am. Nat. 167, 794-807 (2006).

[26]

Jouet, A., McMullan, M. & van Oosterhout, C. The effects of recombination, mutation and selection on the evolution of the Rp1 resistance genes in grasses. Mol. Ecol. 24, 3077-3092 (2015).

[27]

Michelmore, R. W. & Meyers, B. C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8, 1113-1130 (1998).

[28]

Ellstrand, N. C. Is gene flow the most important evolutionary force in plants? Am. J. Bot. 101, 737-753 (2014).

[29]

McMullan, M. et al. Evidence for suppression of immunity as a driver for genomic introgressions and host range expansion in races of Albugo candida, a generalist parasite. eLife 4, e04550 (2015).

[30]

Riaz, S., Lejkina, I., Gubler, W. & Walker, M. Report of a new grape powdery mildew morphotype with branched conidiophores. Plant Pathol. Quar. 3, 19-27 (2013).

[31]

Amrine, K. C. H. et al. Comparative transcriptomics of Central Asian Vitis vinifera accessions reveals distinct defense strategies against powdery mildew. Hortic. Res. 2, 15037 (2015).

[32]

Zohary, D. in The Origins and Ancient History of Wine (eds. Mc Govern, P. E., Fleming, S. J. & Katz, S. H.) Ch. 2 (Gordon and Breach Sciences Publisher, 1995).

[33]

Terral, J. F. et al. Evolution and history of grapevine (Vitis vinifera) under domestication: new morphometric perspectives to understand seed domestication syndrome and reveal origins of ancient European cultivars. Ann. Bot. 105, 443-455 (2010).

[34]

Antcliff, A. J. Inheritance of sex in Vitis. Ann. Amel. Plant 30, 113-122 (1980).

[35]

Massonnet, M. et al. The genetic basis of sex determination in grapevines (Vitis spp.). bioRxiv https://doi.org/10.1101/2019.12.11.861377 (2019).

[36]

Bacilieri, R. et al. Genetic structure in cultivated grapevines is linked to geography and human selection. BMC Plant Biol. 13, 25 (2013).

[37]

Imazio, S. et al. From the cradle of grapevine domestication: molecular overview and description of Georgian grapevine (Vitis vinifera L.) germplasm. Tree Genet. Genomes 9, 641-658 (2013).

[38]

Gaut, B. S. Evolution is an experiment: assessing parallelism in crop domestication and experimental evolution. Mol. Biol. Evol. 32, 1661-1671 (2015).

[39]

Gaut, B. S., Seymour, D. K., Liu, Q. & Zhou, Y. Demography and its effects on genomic variation in crop domestication. Nat. Plants 4, 512-520 (2018).

[40]

Zhou, Y., Massonnet, M., Sanjak, J., Cantu, D. & Gaut, B. S. The evolutionary genomics of grape (Vitis vinifera ssp. vinifera) domestication. Proc. Natl Acad. Sci. USA 114, 11715-11720 (2017).

[41]

Eyre-Walker, A., Gaut, R. L., Hilton, H., Feldman, D. L. & Gaut, B. S. Investigation of the bottleneck leading to the domestication of maize. Proc. Natl Acad. Sci. USA 95, 4441-4446 (1998).

[42]

Tenaillon, M. I., U’Ren, J., Tenaillon, O. & Gaut, B. S. Selection versus demography: a multilocus investigation of the domestication process in maize. Mol. Biol. Evol. 21, 1214-1225 (2004).

[43]

Abbott, R. et al. Hybridization and speciation. J. Evol. Biol. 26, 229-246 (2013).

[44]

Arnold, M. L. & Kunte, K. Adaptive genetic exchange: a tangled history of admixture and evolutionary innovation. Trends Ecol. Evol. 32, 601-611 (2017).

[45]

Marrano, A., Micheletti, D., Lorenzi, S., Neale, D. & Grando, S. Genomic signatures of different adaptations to environmental stimuli between wild and cultivated Vitis vinifera L. Hortic. Res. 5, 34 (2018).

[46]

Norris, L. C. et al. Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets. Proc. Natl Acad. Sci USA. 112, 815-820 (2015).

[47]

Gittelman, R. M. et al. Archaic hominin admixture facilitated adaptation to out-of-Africa environments. Curr. Biol. 26, 3375-3382 (2016).

[48]

Zhang, W. et al. Hypoxia adaptations in the grey wolf (Canis lupus chanco) from Qinghai-Tibet plateau. PLoS Genet. 10, 7 (2014).

[49]

Miao, B., Wang, Z. & Li, Y. Genomic analysis reveals hypoxia adaptation in the Tibetan mastiff by introgression of the grey wolf from the Tibetan plateau. Mol. Biol. Evol. 34, 734-743 (2016).

[50]

Arnold, B. J. et al. Borrowed alleles and convergence in serpentine adaptation. Proc. Natl Acad. Sci USA. 113, 8320-8325 (2016).

[51]

IPGRI, UPOV, OIV. Descriptors for grapevine (Vitis spp.). (International Union for the Protection of New Varieties of Plants, Geneva, Switzerland/Office International de la Vigne et du Vin, Paris, France/ International Plant Genetic Resources Institute, Rome, 1997).

[52]

Reifschneider, F. J. & Boiteux, L. S. A vacuum-operated settling tower for inoculation of powdery mildew fungi. Phytopathology 78, 1463-1465 (1988).

[53]

Van Ooijen, J . Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet. Res. 93, 343-349 (2011).

[54]

Kosambi, D. D. The estimation of map distances from recombination values. Ann. Eugen. 12, 172-175 (1944).

[55]

Van Ooijen, J . MapQTL® 6.0: Software for the mapping of quantitative trait loci in experimental populations of diploid species. (Kyazma B.V., Wageningen, 2009).

[56]

Park, S. D. E. Trypanotolerance in West African Cattle and The Population Genetic Effects of Selection. PhD thesis, University of Dublin. (2001).

[57]

Perrier X., Jacquemoud-Collet J.-P. : DARwin software http://darwin.cirad.fr/darwin (2006)

PDF (1200KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/