Marker-Assisted Evaluation of Two Powdery Mildew Resistance Candidate Genes in Korean Cucumber Inbred Lines
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials and Cultivation
2.2. Evaluation of PM Response
2.3. Genomic DNA Isolation and Molecular Marker Design
2.4. Genotyping of Cucumber Inbred Lines
3. Results and Discussion
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Liu, L.Z.; Yuan, X.J.; Cai, R.; Pan, J.S.; He, H.L.; Yuan, L.H.; Guan, Y.; Zhu, L.H. Quantitative trait loci for resistance to powdery mildew in cucumber under seedling spray inoculation and leaf disc infection. J. Phytopathol. 2008, 156, 691–697. [Google Scholar]
- Huang, S.; Li, R.; Zhang, Z.; Li, L.; Gu, X.; Fan, W. The genome of the cucumber, Cucumis sativus L. Nat. Genet. 2009, 41, 1275–1281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bardin, M.; Carlier, J.; Nicot, P.C. Genetic differentiation in the French population of Erysiphe cichoracearum, a causal agent of powdery mildew of cucurbits. Plant Pathol. 1999, 48, 531–540. [Google Scholar] [CrossRef]
- Bertrand, F. Powdery Mildews of Cucurbits: Pure Culture, Variability and Study of Susceptibility in the Muskmelon Species. Ph.D. Thesis, University of Paris XI, Orsay, France, 1991. [Google Scholar]
- Del-Pino, D.; Olalla, L.; Pérez-García, A.; Rivera, M.E.; García, S.; Moreno, R. Occurrence of races and pathotypes of cucurbit powdery mildew in southeastern Spain. Phytoparasitica 2002, 30, 459–466. [Google Scholar] [CrossRef]
- He, X.M.; Li, Y.H.; Pandey, S.; Yandell, B.S.; Pathak, M.; Weng, Y. QTL mapping of powdery mildew resistance in WI 2757 cucumber (Cucumis sativus L.). Theor. Appl. Genet. 2013, 126, 2149–2161. [Google Scholar] [CrossRef]
- Hosoya, K.; Narisawa, K.; Pitrat, M.; Ezura, H. Race identification in powdery mildew (Sphaerotheca fuliginea) on melon (Cucumis melo) in Japan. Plant Breed. 1999, 118, 259–262. [Google Scholar] [CrossRef]
- Kooistra, E. Powdery mildew resistance in cucumber. Euphytica 1968, 17, 236–244. [Google Scholar] [CrossRef]
- Lee, J.H.; Jang, K.S.; Lee, W.J.; Choi, Y.H. Resistance of cucurbits to Podosphaera xanthii Race 1. Korean J. Hortic. Sci. Technol. 2014, 673–683. [Google Scholar] [CrossRef] [Green Version]
- Pérez-García, A.; Romero, D.; Fernández-Ortuño, D.; López-Ruiz, F.; De Vicente, A.; Tores, J.A. The powdery mildew fungus Podosphaera fusca (synonym Podosphaera xanthii), a constant threat to cucurbits. Mol. Plant Pathol. 2009, 10, 153–160. [Google Scholar] [CrossRef]
- Vakalounakis, D.J.; Klironomou, E.; Papadakis, A. Species spectrum, host range and distribution of powdery mildews on Cucurbitaceae in Crete. Plant Pathol. 1994, 43, 813–818. [Google Scholar] [CrossRef]
- Vakalounakis, D.J.; Klironomou, E. Race and mating type identification of powdery mildew on cucurbits in Greece. Plant Pathol. 1995, 44, 1033–1038. [Google Scholar] [CrossRef]
- Hollomon, D.W.; Wheeler, I.E. Controlling powdery mildews with chemistry. In The Powdery Mildews. A Comprehensive Treatise; Bélanger, R.R., Bushnell, W.R., Dik, A.J., Carver, T.L.W., Eds.; APS Press: Saint Paul, MN, USA, 2002; pp. 249–255. [Google Scholar]
- Innark, P.; Ratanachan, T.; Khanobdee, C.; Samipak, S.; Jantasuriyarat, C. Downy mildew resistant/susceptible cucumber germplasm (Cucumis sativus L.) genetic diversity assessment using ISSR markers. Crop Prot. 2014, 60, 56–61. [Google Scholar] [CrossRef]
- McGrath, M.T. Fungicide Resistance in Cucurbit Powdery Mildew: Experiences and Challenges. Plant Dis. 2001, 85, 236–245. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nie, J.; He, H.; Peng, J.; Yang, X.; Bie, B.; Zhao, J.; Wang, Y.; Si, L.; Pan, J.S.; Cai, R. Identification and fine mapping of pm5.1: A recessive gene for powdery mildew resistance in cucumber (Cucumis sativus L.). Mol. Breed. 2015, 35, 7. [Google Scholar] [CrossRef]
- Nie, J.; Wang, Y.; He, H.; Guo, C.; Zhu, W.; Pan, J.; Li, D.; Lian, H.; Pan, J.; Cai, R. Loss-of-Function Mutations in CsMLO1 Confer Durable Powdery Mildew Resistance in Cucumber (Cucumis sativus L.). Front. Plant Sci. 2015, 6, 1155. [Google Scholar] [CrossRef]
- Schroeder, W.T.; Provvidenti, R. Resistance to benomyl in powdery mildew of cucurbits. Plant Dis. Rep. 1969, 53, 271–275. [Google Scholar]
- Fukino, N.; Yoshioka, Y.; Sugiyama, M.; Sakata, Y.; Matsumoto, S. Identification and validation of powdery mildew (Podosphaera xanthii)-resistant loci in recombinant inbred lines of cucumber (Cucumis sativus L.). Mol. Breed. 2013, 32, 267–277. [Google Scholar] [CrossRef]
- De Ruiter, W.; Hofstede, R.; de Vries, J.; van den Heuvel, H. Combining QTL for resistance to CYSDV and powdery mildew in a single cucumber line. In Proceedings of the 9th EUCARPIA Meeting on Genetics and Breeding of Cucurbitaceae, Avignon, France, 21–24 May 2008; Pitrat, M., Ed.; INRA: Avignon, France, 2008. [Google Scholar]
- Sakata, Y.; Kubo, N.; Morishita, M.; Kitadani, E.; Sugiyama, M.; Hirai, M. QTL analysis of powdery mildew resistance in cucumber. Theor. Appl. Genet. 2006, 112, 243–250. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; VandenLangenberg, K.; Wen, C.; Wehner, T.C.; Weng, Y.Q. QTL mapping of downy and powdery mildew resistances in PI 197088 cucumber with genotyping-by-sequencing in RIL population. Theor. Appl. Genet. 2018, 131, 597–611. [Google Scholar] [CrossRef]
- Zhang, S.P.; Liu, M.M.; Miao, H.; Zhang, S.Q.; Yang, Y.H.; Xie, B.Y.; Gu, X.F. QTL mapping of resistance genes to powdery mildew in cucumber (Cucumis sativus L.). Sci. Agric. Sin. 2011, 44, 3584–3593. [Google Scholar]
- Xu, X.; Yu, T.; Xu, R.; Shi, Y.; Lin, X.; Xu, Q.; Qi, X.; Weng, Y.; Chen, X. Fine mapping of a dominantly inherited powdery mildew resistance major-effect QTL, Pm1.1, in cucumber identifies a 41.1kb region containing two tandemly arrayed cysteine-rich receptor-like protein kinase genes. Theor. Appl. Genet. 2016, 129, 507–516. [Google Scholar] [CrossRef] [PubMed]
- Zhang, K.; Wang, X.; Zhu, W.; Qin, X.; Xu, J.; Cheng, C.; Lou, Q.; Li, J.; Chen, J. Complete resistance to powdery mildew and partial resistance to downy mildew in a Cucumis hystrix introgression line of cucumber were controlled by a co-localized locus. Theor. Appl. Genet. 2018, 131, 2229–2243. [Google Scholar] [CrossRef] [PubMed]
- Berg, J.A.; Appiano, M.; Bijsterbosch, G.; Visser, R.G.F.; Schouten, H.J.; Bai, Y. Functional characterization of cucumber (Cucumis sativus L.) Clade V MLO genes. BMC Plant Biol. 2017, 17, 80. [Google Scholar] [CrossRef]
- Berg, J.A.; Appiano, M.; Santillan-Martinez, M.; Hermans, F.W.; Vriezen, W.H.; Visser, R.G.; Bai, Y.; Schouten, H.J. A transposable element insertion in the susceptibility gene CsaMLO8 results in hypocotyl resistance to powdery mildew in cucumber. BMC Plant Biol. 2015, 15, 243. [Google Scholar] [CrossRef] [Green Version]
- Zhang, C.; Badri Anarjan, M.; Win, K.T.; Begum, S.; Lee, S. QTL-seq analysis of powdery mildew resistance in a Korean cucumber inbred line. Theor. Appl. Genet. 2021, 134, 435–451. [Google Scholar] [CrossRef] [PubMed]
- Ren, Y.; Zhang, Z.; Liu, J.; Staub, J.E.; Han, Y. An Integrated Genetic and Cytogenetic Map of the Cucumber Genome. PLoS ONE 2009, 4, e5795. [Google Scholar] [CrossRef]
- Izumikawa, Y.; Kuzuya, M.; Takazusu, Y.; Miyagi, M. Occurrence of several pathogenic strains of melon powdery mildew with different host-specificity and search for melon breeding materials resistant to these strains. In Proceedings of the 114th Meeting of the Japanese Society of Breeding, Shiga, Japan, 11–12 October 2008. [Google Scholar]
- Jagger, I.C.; Whitaker, T.W.; Porter, D.R. A new biologic form of powdery mildew on muskmelons in the Imperial Valley of California. Plant Dis. Rep. 1938, 22, 275–276. [Google Scholar]
- Kenigsbuch, D.; Cohen, Y. Inheritance and allelism of genes for resistance to races 1 and 2 of Sphaerotheca fuliginea in muskmelon. Plant Dis. 1992, 76, 626–629. [Google Scholar] [CrossRef]
- Kim, H.; Park, J.; Noi, I. Identification of fungal races that cause powdery mildew in melon (Cucumis melo L.) and selection of resistant commercial melon cultivars against the identified races in Korea. J. Plant Biotechnol. 2016, 43, 58–65. [Google Scholar] [CrossRef]
- Kuzuya, M.; Yashiro, K.; Tomita, K. Melon breeding for resistance to powdery mildew in respect to its races. Proc. Veg. Tea Sci. 2004, 1, 39–43. [Google Scholar]
- Pitrat, M.; Dogimont, C.; Bardin, M. Resistance to fungal diseases of foliage in melon. In Cucurbitaceae ’98 Evaluation and Enhancement of Cucurbit Germplasm; McCreight, J.D., Ed.; ASHS Press: Alexandria, VA, USA, 1998; pp. 167–173. [Google Scholar]
- Pryor, D.E.; Whitaker, T.W.; Davis, G.N. The development of powdery mildew resistant cantaloupes. Proc. Am. Soc. Hortic. Sci. 1946, 47, 347–356. [Google Scholar]
Crossing Combination | Types of PM Resistance Source | |
---|---|---|
Resistance Source | Susceptible Source | |
CA/794 (♀) | GHDHW (♂) | A |
2K79 (♀) | HD (♂) | B |
64E2K9 (♀) | HD (♂) | C |
2JKJ (♀) | LC (♂) | D |
249 (♂) | LC (♀) | E |
253XNH (♂) | CPA (♀) | F |
K9AKJ (♀) | CPA (♂) | G |
64E3K9 (♀) | RV (♂) | H |
045911 (♀) | RV (♂) | I |
KJK9 (♀) | CPA (♂) | J |
JCDS (♂) | FPDN (♀) | K |
02789AGN (♂) | MDS (♀) | L |
Line No. | Generation a | Resistance Source h | Phenotypic Evaluation (PE) b | CsaMLO8c | PE vs. CsaMLO8 d | CsLRR-RPK2e | PE vs. CsLRR-RPK2 f | CsaMLO8 vs. CsLRR-RPK2 g |
---|---|---|---|---|---|---|---|---|
DS 1 | 8 | - | S | S | True | S | True | True |
DS 2 | 9 | - | S | S | True | S | True | True |
DS 3 | 9 | - | S | S | True | S | True | True |
DS 4 | 9 | - | S | S | True | S | True | True |
DS 5 | 9 | - | S | S | True | S | True | True |
DS 6 | 5 | - | S | S | True | S | True | True |
DS 7 | 5 | - | S | S | True | S | True | True |
DS 8 | 5 | - | S | S | True | S | True | True |
DS 9 | 5 | - | S | S | True | S | True | True |
DS 10 | 5 | - | S | S | True | S | True | True |
DS 11 | 5 | - | S | S | True | S | True | True |
DS 12 | 5 | - | S | S | True | S | True | True |
DS 13 | 5 | - | S | S | True | S | True | True |
DS 14 | 5 | - | S | S | True | S | True | True |
DS 15 | 9 | - | S | S | True | S | True | True |
DS 16 | 9 | - | S | S | True | S | True | True |
DS 17 | 9 | - | S | S | True | S | True | True |
DS 18 | 9 | - | S | S | True | S | True | True |
DS 19 | 5 | - | S | S | True | S | True | True |
DS 20 | 5 | - | S | S | True | S | True | True |
DS 21 | 5 | - | S | S | True | S | True | True |
DS 22 | 5 | - | S | S | True | S | True | True |
DS 23 | 5 | - | S | S | True | S | True | True |
DS 24 | 5 | - | S | S | True | S | True | True |
DS 25 | 5 | - | S | S | True | S | True | True |
DS 26 | 5 | - | S | S | True | S | True | True |
DS 27 | 7 | - | S | S | True | S | True | True |
DS 28 | 7 | - | S | S | True | S | True | True |
DS 29 | 7 | - | S | S | True | S | True | True |
DS 30 | P | - | S | S | True | S | True | True |
DS 31 | 8 | - | S | S | True | S | True | True |
DS 32 | 8 | - | S | S | True | S | True | True |
DS 33 | 8 | - | S | S | True | S | True | True |
DS 34 | 8 | - | S | S | True | S | True | True |
DS 35 | 9 | - | S | S | True | S | True | True |
DS 68 | 7 | A | R | S | False | R | True | False |
DS 72 | 6 | B | R | R | True | R | True | True |
DS 86 | 6 | C | R | R | True | R | True | True |
DS 88 | 6 | C | R | R | True | S | False | False |
DS 92 | 6 | D | R | R | True | R | True | True |
DS 101 | 5 | D | R | S | False | R | True | False |
DS 102 | 5 | D | R | S | False | R | True | False |
DS 103 | 5 | D | R | S | False | R | True | False |
DS 106 | 5 | D | R | R | True | R | True | True |
DS 111 | 5 | D | R | R | True | R | True | True |
DS 112 | 5 | D | R | R | True | R | True | True |
DS 114 | 5 | D | R | R | True | S | False | False |
DS 115 | 5 | D | R | R | True | R | True | True |
DS 116 | 5 | D | R | R | True | R | True | True |
DS 117 | 5 | D | R | R | True | R | True | True |
DS 119 | 5 | D | R | R | True | R | True | True |
DS 121 | 5 | C | R | R | True | S | False | False |
DS 122 | 5 | C | R | R | True | R | True | True |
DS 123 | 5 | D | R | R | True | R | True | True |
DS 124 | 5 | H | R | R | True | R | True | True |
DS 125 | 5 | H | R | R | True | R | True | True |
DS 126 | 5 | H | R | R | True | S | False | False |
DS 128 | 4 | E | R | R | True | R | True | True |
DS 129 | 4 | E | R | R | True | R | True | True |
DS 130 | 4 | E | R | R | True | R | True | True |
DS 131 | 4 | E | R | R | True | R | True | True |
DS 133 | 4 | E | R | R | True | R | True | True |
DS 195 | 6 | F | R | S | False | R | True | False |
DS 196 | 6 | F | R | S | False | R | True | False |
DS 197 | 4 | G | R | S | False | R | True | False |
DS 198 | 4 | G | R | R | True | R | True | True |
DS 200 | 4 | H | R | R | True | R | True | True |
DS 201 | 4 | H | R | R | True | S | False | False |
DS 202 | 4 | H | R | R | True | S | False | False |
DS 204 | 4 | H | R | R | True | S | False | False |
DS 205 | 4 | H | R | S | False | R | True | False |
DS 206 | 4 | H | R | S | False | R | True | False |
DS 208 | 4 | H | R | R | True | R | True | True |
DS 209 | 4 | H | R | S | False | R | True | False |
DS 211 | 4 | C | R | R | True | R | True | True |
DS 212 | 4 | C | R | S | False | R | True | False |
DS 213 | 4 | C | R | R | True | R | True | True |
DS 214 | 4 | C | R | R | True | R | True | True |
DS 215 | 4 | C | R | S | False | S | False | True |
DS 216 | 4 | C | R | R | True | R | True | True |
DS 217 | 4 | C | R | R | True | S | False | False |
DS 219 | 4 | C | R | S | False | S | False | True |
DS 221 | 3 | I | R | R | True | S | False | False |
DS 223 | 3 | I | R | S | False | S | False | True |
DS 225 | 3 | I | R | S | False | S | False | True |
DS 229 | 3 | J | R | S | False | R | True | False |
DS 234 | 3 | J | R | S | False | R | True | False |
DS 235 | 3 | J | R | S | False | R | True | False |
DS 241 | 3 | C | R | S | False | S | False | True |
DS 340 | 9 | K | R | S | False | R | True | False |
DS 341 | 9 | K | R | S | False | R | True | False |
DS 389 | 4 | L | R | S | False | R | True | False |
DS 394 | 4 | L | R | S | False | S | False | True |
DS 396 | 4 | L | R | S | False | R | True | False |
DS 398 | 4 | L | R | S | False | R | True | False |
DS 417 | 3 | M | S | R | False | S | True | False |
DS 420 | 3 | M | S | R | False | S | True | False |
DS 424 | 3 | L | R | S | False | S | False | True |
DS 425 | 3 | L | R | S | False | R | True | False |
DS 429 | 3 | M | S | R | False | S | True | False |
Name of Gene | Marker Types | Restriction Enzyme | Forward Sequence (5′ to 3′) | Reverse Sequence (5′ to 3′) |
---|---|---|---|---|
CsLRR-RPK2 | CAPS | HinfI | GCAACAAGTTCAATGGACCAC | GAATCTCTCCAGTCAAATTGTTTCC |
CsaMLO8 | InDel | - | TATGGCTGCCTTTCATCTCCT | TCCAAGCAAAGAAGGCAAGC |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Badri Anarjan, M.; Bae, I.; Lee, S. Marker-Assisted Evaluation of Two Powdery Mildew Resistance Candidate Genes in Korean Cucumber Inbred Lines. Agronomy 2021, 11, 2191. https://doi.org/10.3390/agronomy11112191
Badri Anarjan M, Bae I, Lee S. Marker-Assisted Evaluation of Two Powdery Mildew Resistance Candidate Genes in Korean Cucumber Inbred Lines. Agronomy. 2021; 11(11):2191. https://doi.org/10.3390/agronomy11112191
Chicago/Turabian StyleBadri Anarjan, Mahdi, Ikhyun Bae, and Sanghyeob Lee. 2021. "Marker-Assisted Evaluation of Two Powdery Mildew Resistance Candidate Genes in Korean Cucumber Inbred Lines" Agronomy 11, no. 11: 2191. https://doi.org/10.3390/agronomy11112191