Abstract
Key message
Discovery of two rust resistance genes, R17 and R18, from the sunflower lines introduced from South Africa and genetic map** of them to sunflower chromosome 13.
Abstract
Rust, caused by the fungus Puccinia helianthi Schw., is one of the most serious diseases of sunflower in the world. The rapid changes that occur in the virulence characteristics of pathogen populations present a continuous threat to the effectiveness of existing rust-resistant hybrids. Thus, there is a continued need for the characterization of genetically diverse sources of rust resistance. In this study, we report to identify two new rust resistance genes, R17 and R18, from the sunflower lines, KP193 and KP199, introduced from South Africa. The inheritance of rust resistance was investigated in both lines using two map** populations developed by crossing the resistant plants selected from KP193 and KP199 with a common susceptible parent HA 89. The F2 populations were first genotyped using genoty** by sequencing for map** of the rust genes and further saturated with markers in the target region. Molecular map** positioned the two genes at the lower end of sunflower chromosome 13 within a large gene cluster. Two co-segregating SNP markers, SFW01497 and SFW08875, were distal to R17 at a 1.9 cM genetic distance, and a cluster of five co-segregating SNPs was proximal to R17 at 0.7 cM. R18 co-segregated with the SNP marker SFW04317 and was proximal to two cosegregating SNPs, SFW01497 and SFW05453, at 1.9 cM. These maps provide markers for stacking R17 or R18 with other broadly effective rust resistance genes to extend the durability of rust resistance. The relationship of the six rust resistance genes in the cluster was discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bachlava E, Radwan OE, Abratti G, Tang S, Gao W, Heesacker AF, Bazzalo ME, Zambelli A, Leon AJ, Knapp SJ (2011) Downy mildew (Pl8 and Pl14) and rust (RAdv) resistance genes reside in close proximity to tandemly duplicated clusters of non-TIR-like NBS-LRR-encoding genes on sunflower chromosomes 1 and 13. Theor Appl Genet 122:1211–1221. https://doi.org/10.1007/s00122-010-1525-0
Bowers JE, Bachlava E, Brunick RL, Rieseberg LH, Knapp SJ, Burke JM (2012) Development of a 10,000 locus genetic map of the sunflower genome based on multiple crosses. G3-Genes Genom Genet 2:721–729. https://doi.org/10.1534/g3.112.002659
Bulos M, Vergani PN, Altieri E (2014) Genetic map**, marker assisted selection and allelic relationships for the Pu6 gene conferring rust resistance in sunflower. Breed Sci 64:206–212. https://doi.org/10.1270/jsbbs.64.206
de Romano AB, Vázquez AN (2003) Origin of the Argentine sunflower varieties. Helia 26:127. https://doi.org/10.2298/hel0338127d
Dodds PN, Lawrence GJ, Catanzariti A-M, Teh T, Wang C-IA, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103:8888–8893. https://doi.org/10.1073/pnas.0602577103
Ellis JG, Lawrence GJ, Luck JE, Dodds PN (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11:495–506. https://doi.org/10.1105/tpc.11.3.495
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genoty**-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379. https://doi.org/10.1371/journal.pone.0019379
Friskop AJ, Gulya TJ, Halley SA, Schatz BG, Schaefer JP, Jordahl JG, Meyer SM, Misek KW, Hendrickson P, Markell SG (2015a) Effect of fungicide and timing of application on management of sunflower rust. Plant Dis 99:1210–1215. https://doi.org/10.1094/pdis-10-14-1036-re
Friskop AJ, Gulya TJ, Harveson RM, Humann RM, Acevedo M, Markell SG (2015b) Phenotypic diversity of Puccinia helianthi (sunflower rust) in the United States from 2011 and 2012. Plant Dis 99:1604–1609. https://doi.org/10.1094/pdis-11-14-1127-re
Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genoty** by sequencing analysis pipeline. PLoS ONE 9:e90346. https://doi.org/10.1371/journal.pone.0090346
Gong L, Gulya TJ, Markell SG, Hulke BS, Qi LL (2013a) Genetic map** of rust resistance genes in confection sunflower line HA-R6 and oilseed line RHA 397. Theor Appl Genet 126:2039–2049. https://doi.org/10.1007/s00122-013-2116-7
Gong L, Hulke BS, Gulya TJ, Markell SG, Qi LL (2013b) Molecular tagging of a novel rust resistance gene R12 in sunflower (Helianthus annuus L.). Theor Appl Genet 126:93–99. https://doi.org/10.1007/s00122-012-1962-z
Goulter, K. C. (1990) Breeding of a rust differential sunflower line. In: J. K. Kochman (ed.) Proc. of the 8th Australian Sunflower Association Workshop, 19–22 March, 1990. Australian Sunflower Association, Toowoomba, Australia, pp. 120–124
Gulya TJ (1985) Registration of five disease-resistant sunflower germplasms. Crop Sci 25:719–720. https://doi.org/10.2135/cropsci1985.0011183X002500040058x
Gulya TJ, Markell S (2009) Sunflower rust status-2008 race frequency across the Midwest and resistance among commercial hybrids. In: 31st Sunflower Research Forum, January 13–14, 2009, Fargo, ND. National Sunflower Association. Available: http://www.sunflowernsa.com/uploads/Gulya_RustStatus_09.pdf. Accessed August 25, 2020
Gulya TJ, Venette R, Venette JR, Lamey HA (1990). Sunflower rust. NDSU Extension Service Bulletin, Fargo, ND. pp 988. Available: https://library.ndsu.edu/ir/bitstream/handle/10365/5283/pp998.pdf?sequence=1&isAllowed=y. Accessed August 25, 2020
Gulya TJ, Mathew F, Harveson R, Markell S, Block C (2016) Diseases of sunflower. In: McGovern R, Elmer W (eds) Handbook of Florists’ Crops Diseases, Handbook of Plant Disease Management. Springer International Publishing, Cham. https://doi.org/10.1007/978-3-319-32374-9_27-1
Gulya TJ, Harveson R, Mathew F, Block CC, Thompson S, Kandel H, Berglund D, Sandbakken J, Kleingartner L, Markell S (2019) Comprehensive disease survey of U.S. sunflower: disease trends, research priorities and unanticipated impacts. Plant Dis 103:601–618. https://doi.org/10.1094/PDIS-06-18-0980-FE
Islam MR, Shepherd KW (1991) Present status of genetics of rust resistance in flax. Euphytica 55:255–267. https://doi.org/10.1007/BF00021246
Jan C-C, Gulya TJ (2006) Registration of a sunflower germplasm resistant to rust, downy mildew, and virus. Crop Sci 46:1829–1829. https://doi.org/10.2135/cropsci2005.12-0509
Jan CC, Quresh Z, Gulya TJ (2004) Registration of seven rust resistance sunflower germplasms. Crop Sci 44:1887–1888
Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugen 12:172–175. https://doi.org/10.1111/j.1469-1809.1943.tb02321.x
Lambrides CJ, Miller JF (1994) Inheritance of rust resistance in a source of MC29 sunflower germplasm. Crop Sci 34:1225–1230
Lawson WR, Goulter KC, Henry RJ, Kong GA, Kochman JK (1998) Marker-assisted selection for two rust resistance genes in sunflower. Mol Breed 4:227–234. https://doi.org/10.1023/A:1009667112088
Liu Z, Zhang L, Ma GJ, Seiler GJ, Jan CC, Qi LL (2019) Molecular map** of the downy mildew and rust resistance genes in a sunflower germplasm line TX16R. Mol Breed 39:19. https://doi.org/10.1007/s11032-018-0921-z
Long YM, Chao WS, Ma GJ, Xu SS, Qi LL (2017) An innovative SNP genoty** method adapting to multiple platforms and throughputs. Theor Appl Genet 130:597–607. https://doi.org/10.1007/s00122-016-2838-4
Ma GJ, Seiler GJ, Markell SG, Gulya TJ, Qi LL (2016) Registration of two double rust resistant germplasms, HA-R12 and HA-R13 for confection sunflower. J Plant Regist 10:69–74. https://doi.org/10.3198/jpr2015.05.0033crg
Ma GJ, Markell SG, Song QJ, Qi LL (2017) Genoty**-by-sequencing targeting of a novel downy mildew resistance gene Pl20 from wild Helianthus argophyllus for sunflower (Helianthus annuus L.). Theor Appl Genet 130:1519–1529. https://doi.org/10.1007/s00122-017-2906-4
Ma GJ, Song QJ, Markell SG, Qi LL (2018) High-throughput genoty**-by-sequencing facilitates molecular tagging of a novel rust resistance gene, R15, in sunflower (Helianthus annuus L.). Theor Appl Genet 131:1423–1432. https://doi.org/10.1007/s00122-018-3087-5
Ma GJ, Song QJ, Underwood WR, Zhang Z, Fiedler JD, Li X, Qi LL (2019) Molecular dissection of resistance gene cluster and candidate gene identification of Pl17 and Pl19 in sunflower by whole-genome resequencing. Sci Rep 9:14974. https://doi.org/10.1038/s41598-019-50394-8
Ma GJ, Long YM, Song QJ, Talukder ZI, Shamimuzzaman M, Qi LL (2021) Map and sequence-based chromosome walking towards cloning of the male fertility restoration gene Rf5 linked to R11 in sunflower. Sci Rep 11:777
Malav AK, Indu, Chandrawat KS (2016). Gene pyramiding: an overview. Int J Curr Res Biosci Plant Biol, 3: 22–28, https://doi.org/https://doi.org/10.20546/ijcrbp.2016.307.004
Markell S, Gulya TJ, McKay K, Hutter M, Hollingsworth C, Ulstad V, Koch R, Knudsvig A (2009) Widespread occurrence of the aecial stage of sunflower rust caused by Puccinia helianthi in North Dakota and Minnesota in 2008. Plant Dis 93:668–668. https://doi.org/10.1094/PDIS-93-6-0668C
Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61. https://doi.org/10.1146/annurev.arplant.54.031902.135035
Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130. https://doi.org/10.1101/gr.8.11.1113
Miller JF, Gulya TJ (1988) Registration of six downy mildew resistant sunflower germplasm lines. Crop Sci 28:1040–1041
Miller JF, Gulya TJ (1997) Registration of eight maintainer (HA 393, HA 394 and HA 402 to HA 407) and seven restorer (RHA 395 to RHA 401) sunflower germplasm lines. Crop Sci 37:1988–1989. https://doi.org/10.2135/cropsci1997.0011183X003700060069x
Miller JF, Gulya TJ (2001) Registration of three rust resistant sunflower germplasm populations. Crop Sci 41:601–601. https://doi.org/10.2135/cropsci2001.412601x
Moreno PS, de Romano AB, Romano MC, Vergani P, Sposaro M, Bulos M, Altieri E, Ramos ML, Sala CA (2012) A survey of physiological races of Puccinia helianthi in Argentina. In: 18th International Sunflower Conference, Feb 27–March 1, 2012, Mar del Plata, Argentina. International Sunflower Association. pp 87–90
Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BBH, Jones JDG (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91:821–832. https://doi.org/10.1016/S0092-8674(00)80470-5
Putt ED, Sackston WE (1963) Studies on sunflower rust. IV. Two genes, R1 and R2 for resistance in the host. Can J Plant Sci 43:490–496
Qi LL, Ma GJ (2020) Marker-assisted gene pyramiding and the reliability of using SNP markers located in the recombination suppressed regions of sunflower (Helianthus annuus L.). Genes 11:10. https://doi.org/10.3390/genes11010010
Qi LL, Seiler GJ (2013) Registration of a male fertility restorer oilseed sunflower germplasm, HA-R9, resistant to sunflower rust. J Plant Reg 7:353–357
Qi LL, Gulya TJ, Seiler GJ, Hulke BS, Vick BA (2011a) Identification of resistance to new virulent races of rust in sunflowers and validation of DNA markers in the gene pool. Phytopathology 101:241–249. https://doi.org/10.1094/PHYTO-06-10-0162
Qi LL, Hulke BS, Vick BA, Gulya TJ (2011b) Molecular map** of the rust resistance gene R4 to a large NBS-LRR cluster on linkage group 13 of sunflower. Theor Appl Genet 123:351–358. https://doi.org/10.1007/s00122-011-1588-6
Qi LL, Seiler GJ, Vick BA, Gulya TJ (2012) Genetics and map** of the R11 gene conferring resistance to recently emerged rust races, tightly linked to male fertility restoration, in sunflower (Helianthus annuus L.). Theor Appl Genet 125:921–932. https://doi.org/10.1007/s00122-012-1883-x
Qi LL, Ma GJ, Long YM, Hulke BS, Gong L, Markell SG (2015) Relocation of a rust resistance gene R2 and its marker-assisted gene pyramiding in confection sunflower (Helianthus annuus L.). Theor Appl Genet 128:477–488. https://doi.org/10.1007/s00122-014-2446-0
Qi LL, Foley ME, Cai XW, Gulya TJ (2016) Genetics and map** of a novel downy mildew resistance gene, Pl18, introgressed from wild Helianthus argophyllus into cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 129:741–752. https://doi.org/10.1007/s00122-015-2662-2
Radwan O, Gandhi S, Heesacker A, Whitaker B, Taylor C, Plocik A, Kesseli R, Kozik A, Michelmore RW, Knapp SJ (2008) Genetic diversity and genomic distribution of homologs encoding NBS-LRR disease resistance proteins in sunflower. Mol Genet Genomics 280:111–125. https://doi.org/10.1007/s00438-008-0346-1
Sackston WE (1962) Studies on sunflower rust. III. Occurrence, distribution, and significance of race Puccinia helianthi Schw. Can J Bot 40:1449–1458. https://doi.org/10.1139/b62-139
Sendall B, Kong G, Goulter K, Aitken E, Thompson S, Mitchell J, Kochman J, Lawson W, Shatte T, Gulya T (2006) Diversity in the sunflower: Puccinia helianthi pathosystem in Australia. Australas Plant Pathol 35:657–670. https://doi.org/10.1071/AP06071
Talukder ZI, Gong L, Hulke BS, Pegadaraju V, Song Q, Schultz Q, Qi L (2014) A high-density SNP map of sunflower derived from RAD-sequencing facilitating fine-map** of the rust resistance gene R12. PLoS ONE 9:e98628. https://doi.org/10.1371/journal.pone.0098628
Talukder ZI, Ma G, Hulke BS, Jan CC, Qi L (2019) Linkage map** and genome-wide association studies of the Rf gene cluster in sunflower (Helianthus annuus L.) and their distribution in world sunflower collections. Front Genet 10:216. https://doi.org/10.3389/fgene.2019.00216
USDA (2020). Oilseeds: world markets and trade. Foreign Agricultureal Service, United Sates Department of Agriculture. Available: https://apps.fas.usda.gov/psdonline/circulars/oilseeds.pdf. Accessed August, 25, 2020
Van Ooijen JW (2006) JoinMap 4: Software for the calculation of genetic linkage maps in experimental populations of diploid species, 4.1. Kyazma BV, Wageningen, The Netherlands
van Wersch S, Li X (2019) Stronger when together: clustering of plant NLR disease resistance genes. Trends Plant Sci 24:688–699. https://doi.org/10.1016/j.tplants.2019.05.005
Wei F, Wing RA, Wise RP (2002) Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14:1903–1917. https://doi.org/10.1105/tpc.002238
Yang S-M, Antonelli EF, Luciano A, Luciani ND (1986) Reactions of Argentine and Australian sunflower rust differentials to four North American cultures of Puccinia helianthi from North Dakota. Plant Dis 70:883–886
Yang SM, Dowler WM, Luciano A (1989) Gene Pu6: a new gene in sunflower for resistance to Puccinia helianthi. Phytopathol 79:474–477
Yu J-K, Tang S, Slabaugh MB, Heesacker A, Cole G, Herring M, Soper J, Han F, Chu W-C, Webb DM (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43:367–387. https://doi.org/10.2135/cropsci2003.3670
Zhang M, Liu Z, Jan C-C (2016) Molecular map** of a rust resistance gene R14 in cultivated sunflower line PH3. Mol Breed 36:32. https://doi.org/10.1007/s11032-016-0456-0
Zhou B, Dolan M, Sakai H, Wang G-L (2007) The genomic dynamics and evolutionary mechanism of the Pi2/9 locus in rice. Mol Plant-Microbe Interact 20:63–71. https://doi.org/10.1094/mpmi-20-0063
Acknowledgements
We would like to thank Angelia Hogness for technical assistance.
Funding
This project was supported by the USDA-ARS CRIS Project No. 3060-2100-043-00D and the USDA-AMS Specialty Crop Block Grant Programs No. AM200100XXXXG063. Mention of trade names or commercial products in this report is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. The USDA is an equal opportunity provider and employer.
Author information
Authors and Affiliations
Contributions
LLQ conceived and designed the experiments. LLQ, GJM, and XHL performed the experiments. LLQ and TZI analyzed data. LLQ wrote the paper. TZI, XHL, and GJM commented on the manuscript before submission.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical Approval
The experiments were performed in compliance with the current laws of the USA.
Additional information
Communicated by Volker Hahn.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Qi, L.L., Talukder, Z.I., Ma, G.J. et al. Discovery and map** of two new rust resistance genes, R17 and R18, in sunflower using genoty** by sequencing. Theor Appl Genet 134, 2291–2301 (2021). https://doi.org/10.1007/s00122-021-03826-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-021-03826-x