Abstract
A lesion-mimic phenotype appeared in a segregating population of common wheat cross Yanzhan 1/Zaosui 30. The parents had non-lesion normal phenotypes. Shading treatment and histochemical analyses showed that the lesions were caused by light-dependent cell death and were not associated with pathogens. Studies over two cropping seasons showed that some lines with more highly expressed lesion-mimic phenotypes exhibited significantly lower grain yields than those with the normal phenotype, but there were no significant effects in the lines with weakly expressed lesion-mimic phenotypes. Among yield traits, one-thousand grain weight was the most affected by lesion-mimic phenotypes. Genetic analysis indicated that this was a novel type of lesion mimic, which was caused by interaction of recessive genes derived from each parent. The lm1 (lesion mimic 1) locus from Zaosui 30 was flanked by microsatellite markers Xwmc674 and Xbarc133/Xbarc147 on chromosome 3BS, at genetic distances of 1.2 and 3.8 cM, respectively, whereas lm2 from Yanzhan 1 was mapped between microsatellite markers Xgwm513 and Xksum154 on chromosome 4BL, at genetic distances of 1.5 and 3 cM, respectively. The linked microsatellite makers identified in this study might be useful for evaluating whether potential parents with normal phenotype are carriers of lesion-mimic alleles.
Similar content being viewed by others
References
Arase S, Fujita K, Uehara T, Honda Y, Isota J (2000a) Light-enhanced resistance to Magnaporthe grisea infection in the rice sekiguchi lesion mutants. Phytopathology 148(4):197–203
Arase S, Zhao C-M, Akimitsu K, Yamamoto M, Ichii M (2000b) A recessive lesion mimic mutant of rice with elevated resistance to fungal pathogens. J Gen Plant Pathol 66:109–116
Arase S, Ueno M, Toko M (2001) Light-dependent accumulation of tryptamine in the rice Sekiguchi lesion mutant infected with Magnaporthe grisea. Phytopathology 149:409–413
Balagué C, Lin B, Alcon C, Flottes G, Malmstrom S, Kohler C, Neuhaus G, Pelletier G, Gaymard F, Roby D (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15:365–379
Boyd LA, Minchin PN (2001) Wheat mutants showing altered adult plant disease resistance. Euphytica 122:361–368
Boyd LA, Smith PH (2002) Mutations in wheat showing altered field resistance to yellow and brown rust. Genome 45:1035–1040
Brodersen P, Petersen M, Pike HM, Olszak B, Skov S, Odum N, Jorgensen LB, Brown RE, Mundy J (2002) Knockout of Arabidopsis ACCELERATED-CELL-DEATH11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 16:490–502
Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705
Devos KM, Atkinson MD, Chinoy CN, Liu CJ, Gale MD (1992) RFLP-based genetic map of the homoeologous group 3 chromosomes of wheat and rye. Theor Appl Genet 83:931–939
Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL (1994) Arabidopsis mutants simulating disease resistance response. Cell 77:565–577
Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88:685–694
Fu D, Uauy C, Distelfeld A, Blechl A et al (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357–1360
Gray J, Close PS, Briggs SP, Johal GS (1997) A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89:25–31
Gray J, Janick-Buckner D, Buckner B, Close PS, Johal GS (2002) Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol 130:1894–1907
Hu G, Yalpani N, Briggs SP, Johal GS (1998) A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10:1095–1105
Jambunathan N, Siani JM, McNellis TW (2001) A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance. Plant Cell 13:2225–2240
Johal GS, Hulbert SH, Briggs SP (1995) Disease lesion mimics of maize: a model for cell death in plants. BioEssays 17:685–692
Jørgensen JH (1992) Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63:141–152
Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF (2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc Natl Acad Sci USA 98:9448–9453
Kamlofski CA, Antonelli E, Bender C, Jaskelioff M, Danna CH, Ugalde R, Acevedo A (2007) A lesion-mimic mutant of wheat with enhanced resistance to leaf rust. Plant Pathol 56:46–54
Kinane JT, Jones PW (2001) Isolation of wheat mutants with increased resistance to powdery mildew from small induced variant populations. Euphytica 117:251–260
Kinoshita CT (1995) Report of the committee on gene symbolization, nomenclature and linkage groups. Rice Genet Newsl 12:9–115
Kjær B, Jensen HP, Jensen J, Jørgensen JH (1990) Associations between three mlo powdery mildew resistance genes and agronomic traits in barley. Euphytica 46:185–193
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363
Lander ES, Green P, Abrahanson J (1987) MAPMAKER: an interactive computer package maps of experimental and natural populations. Genomics 1:174–181
Li T, Bai G (2009) Lesion mimic associates with adult plant resistance to leaf rust infection in wheat. Theor Appl Genet 119(1):13–21
Li ST, Pei ZY, Luo LJ, Tian YC, He CZ (2005) Isolation and characterization of rice lesion mimic mutants from a T-DNA tagged population. Progr Nat Sci 15:17–23
Li C, Zhu H, Zhang C, Lin F, Xue S, Cao Y, Zhang Z, Zhang L, Ma Z (2008) Mapping QTLs associated with Fusarium-damaged kernels in the Nanda 2419 × Wangshuibai population. Euphytica 163:185–191
Lin F, Xue SL, Zhang ZZ, Zhang CQ, Kong ZX, Yao GQ, Tian DG, Zhu HL, Li CJ, Cao Y, Wei JB, Luo QY, Ma ZQ (2006) Mapping QTL associated with resistance to Fusarium head blight in the Nanda2419 × Wangshuibai population. II: type I resistance. Theor Appl Genet 112:528–535
Lorrain S, Vailleau F, Balague C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8:263–271
Mach JM, Castillo AR, Hoogstraten R, Greenberg JT (2001) The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc Natl Acad Sci USA 98:771–776
Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832
Mou Z, He Y, Dai Y, Liu X, Li J (2000) Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12:405–418
Nair S, Tomar SMS (2001) Genetical and anatomical analyses of a leaf flecking mutant in Triticum aestivum L. Euphytica 121:53–58
Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W, Lagudah E, Somers D, Kilian A, Alaux M, Vautrin S, Berges H, Eversole K, Appels R, Safar J, Simkova H, Dolezel J, Bernard M, Feuillet C (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322:101–104
Pilloff RK, Devadas SK, Enyedi A, Raina R (2002) The Arabidopsis gain-of-function mutant dll1 spontaneously develops lesions mimicking cell death associated with disease. Plant J 30:61–70
Sekiguchi Y, Furuta T (1965) On a rice mutant showing particular reaction to some spotting diseases. Preliminary report. Ann Phytopathol Soc Jpn 30:71–72
Shirano Y, Kachroo P, Shah J, Klessig DF (2002) A gain-of-function mutation in an Arabidopsis Toll Interleukin1 Receptor-Nucleotide Binding Site-Leucine-Rich Repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 14:3149–3162
Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114
Suenaga K, Singh RP, Huerta-Espino J, William HM (2003) Microsatellite markers for genes Lr34/Yr18 and other quantitative trait loci for leaf rust and stripe rust resistance in bread wheat. Phytopathology 93:881–890
Takahashi A, Kawasaki T, Henmi K, Shi IK, Kodama O, Satoh H, Shimamoto K (1999) Lesion mimic mutants of rice with alterations in early signaling events of defense. Plant J 17:535–545
Tixier MH, Sourdille RM, Leroy P, Bernard M (1997) Detection of wheat microsatellites using a non radioactive silver-nitrate staining method. Genet Breed 51:175–177
Walbot V, Hoisington DA, Neuffer MG (1983) Disease lesion mimic mutations. Plenum Publ Corp, New York
William HM, Singh RP, Huerta-Espino J, Palacios G, Suenaga K (2006) Characterization of genetic loci conferring adult plant resistance to leaf rust and stripe rust in spring wheat. Genome 49:977–990
Wu C, Bordeos A, Madamba MR, Baraoidan M, Ramos M, Wang GL, Leach JE, Leung H (2008) Rice lesion mimic mutants with enhanced resistance to diseases. Mol Genet Genomics 279:605–619
Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci USA 99:7530–7535
Yin Z, Chen J, Zeng L, Goh M, Leung H, Khush GS, Wang GL (2000) Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol Plant Microbe Interact 13:869–876
Yoshioka K, Kachroo P, Tsui F, Sharma SB, Shah J, Klessig DF (2001) Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. Plant J 26:447–459
Yu JK, Dake TM, Singh S, Benscher D, Li W, Gill B, Sorrells ME (2004) Development and mapping of EST-derived simple sequence repeat markers for hexaploid wheat. Genome 47:805–818
Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang GL (2004) Spotted leaf 11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16:2795–2808
Acknowledgments
The project was sponsored by the National Basic Research Project of China (2004CB117200). We are grateful to Dr. R. McIntosh, University of Sydney, for useful suggestions on the phenotyping and for revising this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Sorrells.
Rights and permissions
About this article
Cite this article
Yao, Q., Zhou, R., Fu, T. et al. Characterization and mapping of complementary lesion-mimic genes lm1 and lm2 in common wheat. Theor Appl Genet 119, 1005–1012 (2009). https://doi.org/10.1007/s00122-009-1104-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-009-1104-4