Durable Late Blight Resistance in Potato Through Dynamic Varieties Obtained by Cisgenesis: Scientific and Societal Advances in the DuRPh Project

Potato Research - Tập 59 Số 1 - Trang 35-66 - 2016
A. J. Haverkort1, P.M. Boonekamp1, R.C.B. Hutten1, E. Jacobsen1, L.A.P. Lotz1, G.J.T. Kessel1, Jack H. Vossen1, Richard G. F. Visser1
1Wageningen University and Research Centre, P.O. Box 16, 6700 AA, Wageningen, The Netherlands

Tóm tắt

Abstract

From 2006 through 2015, a research project on Durable Resistance in potato against Phytophthora (DuRPh) was carried out at Wageningen University and Research Centre. Its objective was to develop a proof of principle for durable resistance against late blight by cisgenesis. This public-funded project aimed at stimulating research on genetic modification and public debate on innovative genetic techniques. It was decided to clone and transfer late blight resistance (R) genes of crossable wild potato species (cisgenes) by Agrobacterium tumefaciens-mediated transformation without non-potato genes. A stack of multiple R genes were planned to be inserted into established varieties, thereby creating a dynamic variety in which the composition of the stacks may vary over space and time. Cisgenic plants were selected based on the expression of all inserted R genes and trueness-to-type. Within the project, 13 R genes from wild potato species were genetically mapped and three of them were cloned. Four varieties were transformed with one to three R genes. This was initially done using kanamycin resistance provided by a selectable marker gene of synthetic origin in order to quickly test the performance and stability of the introduced R genes and stacked R gene combinations. Once the functioning thereof was confirmed, marker-free transformations were conducted; thus, true cisgenic events were selected. The results about the different R genes, their chromosomal location, their specificity, the background dependence, the maximum size of a stack, its regeneration time and associated somaclonal variation frequency and its stability were studied. After selection and characterisation in the laboratory, the best cisgenic events were assessed in field trials for late blight resistance. This showed that inserted R genes were capable of turning a susceptible variety into a resistant one. Maximising longevity of the resistance was assured through resistance management research. It was shown that stacking of multiple R genes and monitoring how to deploy these stacks spatially and temporally could reduce fungicide use by over 80%. Communications through media and field demonstrations were manifold to allow public and policymakers to decide if cisgenesis is an acceptable tool to make potato farming more sustainable. Future deployment of the DuRPh strategy will depend largely on its status as a genetically modified crop or its exemption thereof. Worldwide near eradication of late blight would increase global annual potato production by close to 80 million tons, thereby contributing considerably to the needed additional global future food supply.

Từ khóa


Tài liệu tham khảo

Anonymus (2013) Landbouweconomisch Bericht. Berkhout, Silvis PH, en Terluin (eds.) LEI-rapport 2013-041ISNN0169-3255, 212 pp

Black W, Mastenbroek C, Mills WR, Peterson LC (1953) A proposal for an international nomenclature of races of Phytophthora infestans and of genes controlling immunity in Solanum demissum derivates. Euphytica 2:173–240

Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR et al. (2012) Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathog 8(10):e1002940. doi:10.1371/journal.ppat.1002940

Cupsa I, Ignatescu I, Vogel E (1983) An epidemic of potato late blight in 1982, and measures taken to prevent it in 1983 (Epidemia de mana a cartofului in anul 1982 si masuri de prevenire a acesteia in anul 1983). Productia Vegetala Horticultura 32:22–26

De Vetten N, Wolters MA, Raemakers K, van der Meer I, ter Stege R, Heeres P, Visser RGF (2003) A transformation method for obtaining marker-free plants of a cross-pollinating and vegetatively propagated crop. Nat Biotechnol 21:439–442

Fry WE (1977) Integrated control of potato late blight: effects of polygenic resistance and techniques of timing fungicide applications. Phytopathology 67:415–420

FAOSTAT 2014, http://faostat.fao.org/default.aspx. Accessed August 2015

Flier WG, Kroon LPNM, Hermansen A, Van Raaij HMG, Speiser B, Tamm L, Fuchs JG, Lambion J, Razzaghian J, Andrivon D, Wilcockson S, Leifert C (2007) Genetic structure and pathogenicity of populations of Phytophthora infestans from organic potato crops in France, Norway, Switzerland and the United Kingdom. Plant Pathol 56:562–572

Flier WG, Turkensteen LJ (1999) Foliar aggressiveness of Phytophthora infestans in three potato growing regions in the Netherlands. Eur J Plant Pathol 105(4):381–388

Fontem DA, Aighewi B (1993) Effect of fungicides on late blight control and yield loss of potato in the western highlands of Cameroon. Int J Pest Manag 39:152–155

Forbes G (2010) Late blight, action plan for an effective response to a global threat. White Paper June http://192.156.137.121:8080/cipotato/publications/pdf/222222.pdf

Grafius EJ, Douches DS (2008) The present and future role of insect-resistant genetically modified potato varieties. In: Romeis J, Shelton AM, Kennedy GG (eds.) Integration of insect-resistant genetically modified crops within IPM programs. pp. 195–205

Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, Bozkurt TO, Ah-Fong AM, Alvarado L, Anderson VL, Armstrong MR, Avrova A, Baxter L, Beynon J, Boevink PC, Bollmann SR, Bos JI, Bulone V, Cai G, Cakir C, Carrington JC, Chawner M, Conti L, Costanzo S, Ewan R, Fahlgren N, Fischbach MA, Fugelstad J, Gilroy EM, Gnerre S, Green PJ, Grenville-Briggs LJ, Griffith J, Grünwald NJ, Horn K, Horner NR, Hu CH, Huitema E, Jeong DH, Jones AM, Jones JD, Jones RW, Karlsson EK, Kunjeti SG, Lamour K, Liu Z, Ma L, Maclean D, Chibucos MC, McDonald H, McWalters J, Meijer HJ, Morgan W, Morris PF, Munro CA, O’Neill K, Ospina-Giraldo M, Pinzón A, Pritchard L, Ramsahoye B, Ren Q, Restrepo S, Roy S, Sadanandom A, Savidor A, Schornack S, Schwartz DC, Schumann UD, Schwessinger B, Seyer L, Sharpe T, Silvar C, Song J, Studholme DJ, Sykes S, Thines M, van de Vondervoort PJ, Phuntumart V, Wawra S, Weide R, Win J, Young C, Zhou S, Fry W, Meyers BC, van West P, Ristaino J, Govers F, Birch PR, Whisson SC, Judelson HS, Nusbaum C (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461(7262):393–398

Haesaert G, Vossen JH, Custers R, De Loose M, Haverkort AJ, Heremans B, Hutten R, Kessel G, Landschoot S, Van Droogenbroeck B, Visser RGF, Gheysen G (2015) Field performance of an established potato variety improved by transformation with multiple late blight resistance genes. Crop Prot 77:163–175

Haldar K, Kamoun S, Hiller NL, Bhattacharje S, van Ooij C (2006) Common infection strategies of pathogenic eukaryotes. Nat Rev Microbiol 4:922–931

Haverkort AJ, Hillier JG (2011) Cool farm tool – potato: model description and performance of four production systems. Potato Res 54:355–369

Haverkort AJ, Boonekamp PM, Hutten R, Jacobsen E, Lotz LAP, Kessel GJT, Visser RGF, van der Vossen AEG (2008) Societal costs of late blight in potato and prospects of durable resistance through cisgenic modification. Potato Res 51:47–57

Haverkort AJ, Struik PC, Visser RGF, Jacobsen E (2009) Applied biotechnology to combat late blight in potato caused by Phytophthora infestans. Potato Res 52:249–264

Higiro J, Danial DL (1994) Potato production in Burundi: constraints and research. In: Proceedings of a regional workshop for Eastern, Central and Southern Africa. Proceedings of a regional workshop for Eastern, Central and Southern Africa, Njoro, Kenya. pp. 117–118

James C (2014) Global status of commercialized biotech/GM crops: 2014. ISAAA Brief No. 49. ISAAA: Ithaca, NY, 325 pp

Jo KR, Arens M, Kim TY, Jongsma MA, Visser RGF, Jacobsen E, Vossen JH (2011) Mapping of the S. demissum late blight resistance gene R8 to a new locus on chromosome IX. Theor Appl Genet 123:1331–1340

Jo K-R (2013) Unveiling and deploying durability of late blight resistance in potato from natural stacking to cisgenic stacking. PhD Thesis, Wageningen University, Wageningen, The Netherlands, p 168

Jo KR, Kim CJ, Kim SJ, Kim TJ, Bergervoet-van Deelen JEM, Jongsma MA, Visser RGF, Jacobsen E, Vossen J (2014) Development of late blight resistant potatoes by cisgenic stacking. BMC Biotechnol 14:1472–6750

Jo KR, Visser RGF, Jacobsen E, Vossen JH (2015) Characterisation of the late blight resistance in potato differential MaR9 reveals a qualitative resistance gene, R9a, residing in a cluster of Tm-2 2 homologs on chromosome IX. Theor Appl Genet 128(5):931–941

Jo K-R, Zhu S, Bai Y, Hutten RCB, Kessel GJT, Vleeshouwers VGAA, Jacobsen E, Visser RGF, Vossen JH (2016) Plant pathogen resistance biotechnology. In: Collinge DB (ed) Wiley-Blackwell. pp. 448

Judelson HS, Blanco F (2005) The spores of Phytophthora weapons of the plant destroyer. Nat Rev Microbiol 3:47–57

Jupe F, Witek K, Verweij W, Śliwka J, Pritchard L, Etherington GJ, Maclean D, Cock PJ, Leggett RM, Bryan GJ, Cardle L, Hein I, Jones JDG (2013) Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. The Plant Journal 76(3):530–544

Kim HJ, Lee HR, Jo KR, Mahdi Mortazavian SM, Huigen DJ, Evenhuis B, Kessel G, Visser RGF, Jacobsen E, Vossen JH (2012) Broad spectrum late blight resistance in potato differential set plants MaR8 and MaR9 is conferred by multiple stacked R genes. Theor Appl Genet 124:923–935

Lalancette N, Ellis MA, Madden LV (1988) Development of an infection efficiency model for Plasmopara viticola on American grape based on temperature and duration of leaf wetness. Phytopathology 78:794–800

Li G, Huang S, Guo X, Li Y, Yang Y, Guo Z, Kuang H, Rietman H, Bergervoet M, Vleeshouwers VGAA, van der Vossen E, Qu D, Visser RGA, Jacobsen E, Vossen JH (2011) Cloning and characterization of R3b; members of the R3 superfamily of late blight resistance genes show sequence and functional divergence. Mol Plant Microbe Interact 24:1132–1142

Lotz LAP, Van de Wiel CCM, Smulders MJM (2014) GM crops and sustainable agriculture: a proposed way forward in the societal debate. NJAS Wageningen J Life Sci 70–71:95–98

Lungaho C, Nyongesa N, Lemaga B (2008) Yield and economic losses caused by potato late blight in Central Kenya. https://research.cip.cgiar.org/confluence/download/attachments/8159378/p20.pdf

Nærstad R, Hermansen A, Bjor T (2007) Exploiting host resistance to reduce the use of fungicides to control potato late blight. Plant Pathol 56:15–166

Pietkiewicz JB (1991) Potato production and protection in Poland in the 1990s. Bull-OEPP 21:1–7

The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195

Rao ANS, Veeresh GK (1989) Estimation of yield loss due to late blight in rainfed potato. Curr Res. University of Agricultural Sciences, Bangalore, 18:157–158

Rietman H, Bijsterbosch G, Cano LM, Lee HR, Vossen JH, Jacobsen E, Visser RGF, Kamoun S, Vleeshouwers VGGA (2012) Qualitative and quantitative late blight resistance in the potato variety Sarpo Mira is determined by the perception of five distinct RXLR effectors. Mol Plant-Microbe Interact 25:910–919

Rodewald J, Trognitz B (2013) Solanum resistance genes against Phytophthora infestans and their corresponding avirulence genes. Mol Plant Pathol 14(7):740–757

Schouten HJ, Krens FA, Jacobsen E (2006) Cisgenic plants are similar to traditionally bred plants: international regulations for genetically modified organisms should be altered to exempt cisgenesis. EMBO Reports 7:750–753

Skelsey P, Rossing WA, Kessel GJT, van der Werf W (2010) Invasion of Phytophthora infestans at the landscape level: how do spatial scale and weather modulate the consequences of spatial heterogeneity in host resistance? Phytopathology 100:1146–1161

Skelsey P, Rossing WAH, Kessel GJT, Powell J, van der Werf W (2005) Influence of host diversity on development of epidemics: an evaluation and elaboration of mixture theory. Phytopathology 95:328–338

Storck T, Böhme T, Schultheiss H (2012) Status and perspectives of GM approaches to fight late blight. Thirteenth EuroBlight workshop, St. Petersburg (Russia), 9–12 October 2011, PPO-Special Report 15:45–48

Taylor J (1973) The analysis of designed experiments with censored observations. Biometrics 29:35–43

Thornton M (2003) The rise and fall of NewLeaf potatoes. NABC Report 15: Biotechnology: Science and Society at a Crossroad, pp. 235–243

Vleeshouwers VGAA, Raffaele S, Vossen JH, Champouret N, Oliva R, Segretin ME, Rietman H, Cano LM, Lokossou AA, Kessel GJT, Pel M, Kamoun S (2011) Understanding and exploiting late blight resistance in the age of effectors. Annu Rev Plant Physiol Plant Mol Biol 49:507–531

Vossen JH, Dezhsetan S, Esselink D, Arens M, Sanz MJ, Verweij W, Verzaux E, van der Linden CG (2013) Novel applications of motif-directed profiling to identify disease resistance genes in plants. BMC Plant Methods 9:37–49

Vossen JH, Nijenhuis M, Arens-de Reuver MJB, van der Vossen EAG, Jacobsen J, Visser RGF (2011). Cloning and exploitation of a functional R gene from Solanum chacoense. Patent number WO/2011/034433

Wang M, Sjefke A, van den Berg RG, Vleeshouwers VGAA, van der Vossen EAG, Vosman B (2008) Allele mining in Solanum: conserved homologues of Rpi-blb1 are identified in Solanum stoloniferum. Theor Appl Genet 116(7):933–943

Xie K, Wang Y (2001) CIP potato late blight research in China. Journal of Agricultural University of Hebei. 8 pp https://research.cip.cgiar.org/confluence/download/attachments/37192022/xiekaiyun_10_pdf?version=1&modificationDate=1273631094000. Accessed August 2015

Zhu S, Duwal A, Su Q, Vossen JH, Visser RGF, Jacobsen E (2013) Vector integration in triple R gene transformants and the clustered inheritance of resistance against potato late blight. Transgenic Res 22(2):315–325

Zhu S, Vossen JH, Bergervoet M, Nijenhuis M, Kodde L, Kessel GJT, Vleeshouwers V, Visser RGF, Jacobsen E (2015) An updated conventional- and a novel GM potato late blight R gene differential set for virulence monitoring of Phytophthora infestans. Euphytica 202(2):219–234