Abstract
Key message
Apart from confinement of Ne1 to a 4.45 Mb genomic segment, markers closely linked to Ne2 were identified and incomplete dominance of both genes in conditioning necrosis severity was shown.
Abstract
Hybrid necrosis in plants is characterized by premature death of leaves or plants in F1 hybrids. Interaction of two complementary dominant genes Ne1 and Ne2 in wheat (Triticum aestivum L.) is known to cause hybrid necrosis. However, the mechanism underlying this necrosis is still elusive. To obtain markers closely-linked to these two genes, Ne1-carrying cultivar Zheng891 was crossed with Ne2-carrying cultivar Pan555. Using BC1F1 plants derived from crosses of the F1 plants with the two parental lines, Ne1 and Ne2 were mapped to a 2.2 cM interval and a 2.3 cM interval with newly developed markers, respectively. Ne1 was further delimited to a 0.19 cM interval using 2015 Ne2-carrying F2 plants. Xwgrc3146, Xwgrc3147 and Xwgrc3150, three of the four markers co-segregating with Ne1, were all Zheng891-dominant, suggesting that, compared with Pan555, Ne1 is located in a region with substantial sequence diversity. The Ne1 interval is syntenic to chromosomes 5H, 4, 9 and 2 of barley, Brachypodium distachyon, rice and sorghum, respectively, and corresponds to a 4.45 Mb Chinese Spring sequence. Variations in necrosis severity of the F2 plants differing in Ne1 and Ne2 genotypes implied that these two genes are incompletely dominant in determining the timing and severity of necrosis.
Similar content being viewed by others
Availability of data and material
Available upon request.
Code availability
Not applicable.
References
Akhunov E, Goodyear A, Geng S, Qi L, Echalier B, Gill B, Miftahudin GJ, Lazo G, Chao S, Anderson O, Linkiewicz A, Dubcovsky J, La Rota M, Sorrells M, Zhang D, Nguyen H, Kalavacharla V, Hossain K, Kianian S, Peng J, Lapitan N, Gonzalez-Hernandez J, Anderson J, Choi D, Close T, Dilbirligi M, Gill K, Walker-Simmons M, Steber C, McGuire P, Qualset C, Dvorak J (2003) The organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms. Genome Res 13:753–763
Alcázar R, García AV, Kronholm I, de Meaux J, Koornneef M, Parker JE, Reymond M (2010) Natural variation at Strubbelig Receptor Kinase 3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions. Nat Genet 42:1135–1139
Alcázar R, von Reth M, Bautor J, Chae E, Weigel D, Koornneef M, Parker JE (2014) Analysis of a plant complex resistance gene locus underlying immune-related hybrid incompatibility and its occurrence in nature. PloS Genet 10:e1004848
Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K, Jordan KW, Golan G, Deek J, Ben-Zvi B, Ben-Zvi G, Himmelbach A, MacLachlan RP, Sharpe AG, Fritz A, Ben-David R, Budak H, Fahima T, Korol A, Faris JD, Hernandez A, Mikel MA, Levy AA, Steffenson B, Maccaferri M, Tuberosa R, Cattivelli L, Faccioli P, Ceriotti A, Kashkush K, Pourkheirandish M, Komatsuda T, Eilam T, Sela H, Sharon A, Ohad N, Chamovitz DA, Mayer KFX, Stein N, Ronen G, Peleg Z, Pozniak CJ, Akhunov ED, Distelfeld A (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97
Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80
Bateson W (1909) Heredity and variation in modern lights. In: Seward AC (ed) Darwin and modern science. Cambridge University Press, Cambridge, pp 85–101
Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8:382–393
Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol 5:e236
Caldwell R, Compton L (1943) Complementary lethal genes in wheat causing a progressive lethal necrosis of seedlings. J Hered 34:67–70
Chen C, E Z, Lin HX, (2016) Evolution and molecular control of hybrid incompatibility in plants. Front Plant Sci 7:1208
Chen C, Chen H, Shan JX, Zhu MZ, Shi M, Gao JP, Lin HX (2013) Genetic and physiological analysis of a novel type of interspecific hybrid weakness in rice. Mol Plant 6:716–728
Chen C, Chen H, Lin YS, Shen JB, Shan JX, Qi P, Shi M, Zhu MZ, Huang XH, Feng Q, Han B, Jiang L, Gao JP, Lin HX (2014) A two-locus interaction causes interspecific hybrid weakness in rice. Nature Commun 5:3357
Choi HW, Kim YJ, Hwang BK (2011) The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity. Mol Plant Microbe Interact 24:68–78
Chu CG, Faris JD, Friesen TL, Xu SS (2006) Molecular mapping of hybrid necrosis genes Ne1 and Ne2 in hexaploid wheat using microsatellite markers. Theor Appl Genet 112:1374–1381
Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York
Dvorák J, Luo M, Yang Z (1998) Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 148:423–434
Guo W, Xin M, Wang Z, Yao Y, Hu Z, Song W, Yu K, Chen Y, Wang X, Guan P, Appels R, Peng H, Ni Z, Sun Q (2020) Origin and adaptation to high altitude of Tibetan semi-wild wheat. Nat Commun 11:5085
Hermsen JGTh (1963a) Hybrid necrosis as a problem for the wheat breeder. Euphytica 12:1–16
Hermsen JGTh (1963b) Sources and distribution of the compiementary genes for hybrid necrosis in wheat. Euphytica 12:147–160
Hermsen JGTh (1963c) The genetic basis of hybrid necrosis in wheat. Genetica 33:245–287
Ichitani K, Namigoshi K, Sato M, Taura S, Aoki M, Matsumoto Y, Saitou T, Marubashi W, Kuboyama T (2007) Fine mapping and allelic dosage effect of Hwc1, a complementary hybrid weakness gene in rice. Theor Appl Genet 114:1407–1415
Ichitani K, Taura S, Tezuka T, Okiyama Y, Kuboyama T (2011) Chromosomal location of HWA1 and HWA2, complementary hybrid weakness genes in rice. Rice 4:29–38
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329
Jung HW, Hwang BK (2007) The leucine-rich repeat (LRR) protein, CaLRR1, interacts with the hypersensitive induced reaction (HIR) protein, CaHIR1, and suppresses cell death induced by the CaHIR1 protein. Mol Plant Pathol 8:503–514
Jung HW, Lim CW, Lee SC, Choi HW, Hwang CH, Hwang BK (2008) Distinct roles of the pepper hypersensitive induced reaction protein gene CaHIR1 in disease and osmotic stress, as determined by comparative transcriptome and proteome analyses. Planta 227:409–425
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Krüger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JD (2002) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296:744–747
Kuboyama T, Saito T, Matsumoto T, Wu J, Kanamori H, Taura S, Sato M, Marubashi W, Ichitani K (2009) Fine mapping of HWC2, a complementary hybrid weakness gene, and haplotype analysis around the locus in rice. Rice 2:93–103
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181
Li M, Li B, Guo G, Chen Y, Xie J, Lu P, Wu Q, Zhang D, Zhang H, Yang J, Zhang P, Zhang Y, Liu Z (2018) Mapping a leaf senescence gene els1 by BSR-Seq in common wheat. Crop J 6:236–243
Liu H, Marubashi W (2014) Species origin of genomic factors in Nicotiana nudicaulis Watson controlling hybrid lethality in interspecific hybrids between N. nudicaulis Watson and N. tabacum L. PloS One 9:e97004
Ma ZQ, Sorrells ME (1995) Genetic analysis of fertility restoration in wheat using restriction fragment length polymorphisms. Crop Sci 35:1137–1143
Maccaferri M, Harris NS, Twardziok SO, Pasam RK, Gundlach H, Spannagl M, Ormanbekova D, Lux T, Prade VM, Milner SG, Himmelbach A, Mascher M, Bagnaresi P, Faccioli P, Cozzi P, Lauria M, Lazzari B, Stella A, Manconi A, Gnocchi M, Moscatelli M, Avni R, Deek J, Biyiklioglu S, Frascaroli E, Corneti S, Salvi S, Sonnante G, Desiderio F, Marè C, Crosatti C, Mica E, Özkan H, Kilian B, De Vita P, Marone D, Joukhadar R, Mazzucotelli E, Nigro D, Gadaleta A, Chao S, Faris JD, Melo ATO, Pumphrey M, Pecchioni N, Milanesi L, Wiebe K, Ens J, MacLachlan RP, Clarke JM, Sharpe AG, Koh CS, Liang KYH, Taylor GJ, Knox R, Budak H, Mastrangelo AM, Xu SS, Stein N, Hale I, Distelfeld A, Hayden MJ, Tuberosa R, Walkowiak S, Mayer KFX, Ceriotti A, Pozniak CJ, Cattivelli L (2019) Durum wheat genome highlights past domestication signatures and future improvement targets. Nat Genet 51:885–895
Minina EA, Filonova LH, Sanchez-Vera V, Suarez MF, Daniel G, Bozhkov PV (2013) Detection and measurement of necrosis in plants. Methods Mol Biol 1004:229–248
Mizuno N, Hosogi N, Park P, Takumi S (2010) Hypersensitive response-like reaction is associated with hybrid necrosis in interspecific crosses between tetraploid wheat and Aegilops tauschii Coss. PLoS ONE 5:e11326
Mizuno N, Shitsukawa N, Hosogi N, Park P, Takumi S (2011) Autoimmune response and repression of mitotic cell division occur in interspecific crosses between tetraploid wheat and Aegilops tauschii Coss. that show low temperature-induced hybrid necrosis. Plant J 68:114–128
Muller HJ (1942) Isolating mechanisms, evolution and temperature. Biol Symp 6:71–124
Muralidharan S, Box MS, Sedivy EL, Wigge PA, Weigel D, Rowan BA (2014) Different mechanisms for Arabidopsis thaliana hybrid necrosis cases inferred from temperature responses. Plant Biol 16:1033–1041
Nishikawa K, Mori T, Takami N, Furuta Y (1974) Mapping of progressive necrosis gene Ne1 and Ne2 of common wheat by the telocentric method. Japan J Breed 24:277–281
Pan X, Pan S, Shi Y, Pan Q, Zhang L, Pan T, Xue Y (2015) Registration of wheat line ShunMai yyAh for hybrid necrosis. J Plant Register 9:407
Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, van Ex F, Pasha A, Khedikar Y, Robinson SJ, Cory AT, Florio T, Concia L, Juery C, Schoonbeek H, Steuernagel B, Xiang D, Ridout CJ, Chalhoub B, Mayer KFX, Benhamed M, Latrasse D, Bendahmane A, IWGSC, Wulff BBH, Appels R, Tiwari V, Datla R, Choulet F, Pozniak CJ, Provart NJ, Sharpe AG, Paux E, Spannagl M, Bräutigam A, Uauy C (2018) The transcriptional landscape of polyploid wheat. Science 361:eaar6089
Rooney W, Stelly D (1990) Genetic effects on the timing of Le2daw induced necrosis of cotton. Crop Sci 30:70–74
Saito T, Ichitani K, Suzeki T, Marubashi W, Kuboyama T (2007) Developmental observation and high temperature rescue from hybrid weakness in a cross between Japanese rice cultivar and Peruvian rice cultivar ‘Jamaica.’ Breed Sci 57:281–288
Sakaguchi K, Nishijima R, Iehisa JC, Takumi S (2016) Fine mapping and genetic association analysis of Net2, the causative D-genome locus of low temperature-induced hybrid necrosis in interspecific crosses between tetraploid wheat and Aegilops tauschii. Genetica 144:523–533
Shii CT, Mok MC, Temple SR, Mok DWS (1980) Expression of developmental abnormalities in hybrids of Phaseolus vulgaris L.: Interaction between temperature and allelic dosage. J Hered 71:218–222
Singh RP, Singh I, Chowdhury RK (1992) Hybrid necrosis in bread wheat. III Wheat Inf Serv 74:22–24
Smith LM, Bomblies K, Weigel D (2011) Complex evolutionary events at a tandem cluster of Arabidopsis thaliana genes resulting in a single-locus genetic incompatibility. PloS Genet 7:e1002164
Song L, Guo W, Zhang T (2009) Interaction of novel Dobzhansky-Muller type genes for the induction of hybrid lethality between Gossypium hirsutum and G. barbadense cv. Coastland R4–4. Theor Appl Genet 119:33–41
Stein N, Feuillet C, Wicker T, Schlagenhauf E, Keller B (2000) Subgenome chromosome walking in wheat: a 450-kb physical contig in Triticum monococcum L. spans the Lr10 resistance locus in hexaploid wheat (Triticum aestivum L.). Proc Natl Acad Sci U S A 97:13436–13441
Świadek M, Proost S, Sieh D, Yu J, Todesco M, Jorzig C, Rodriguez Cubillos AE, Plotner B, Nikoloski Z, Chae E, Giavalisco P, Fischer A, Schroder F, Kim ST, Weigel D, Laitinen RA (2017) Novel allelic variants in ACD6 cause hybrid necrosis in local collection of Arabidopsis thaliana. New Phytol 213:900–915
Takamatsu K, Iehisa JC, Nishijima R, Takumi S (2015) Comparison of gene expression profiles and responses to zinc chloride among inter- and intraspecific hybrids with growth abnormalities in wheat and its relatives. Plant Mol Biol 88:487–502
Takumi S, Motomura Y, Iehisa JCM, Kobayashi F (2013) Segregation distortion caused by weak hybrid necrosis in recombinant inbred lines of common wheat. Genetica 141:463–470
Tezuka T, Marubashi W (2006) Hybrid lethality in interspecific hybrids between Nicotiana tabacum and N. suaveolens: evidence that the Q chromosome causes hybrid lethality based on Q-chromosome-specific DNA markers. Theor Appl Genet 112:1172–1178
Tezuka T, Matsuo C, Iizuka T, Oda M, Marubashi W (2012) Identification of Nicotiana tabacum linkage group corresponding to the Q chromosome gene(s) involved in hybrid lethality. PLoS ONE 7:e37822
Tsunewaki K (1960) Monosomic and conventional gene analysis in common wheat. III Lethality Jpn J Genet 35:71–75
Tsunewaki K (1992) Aneuploid analyses of hybrid necrosis and hybrid chlorosis in tetraploid wheats using the D genome chromosome substitution lines of durum wheat. Genome 35:594–601
van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LA, Petersen M, Smertenko A, Taliansky M, Van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246
Walkowiak S, Gao L, Monat C, Haberer G, Kassa MT, Brinton J, Ramirez-Gonzalez RH, Kolodziej MC, Delorean E, Thambugala D, Klymiuk V, Byrns B, Gundlach H, Bandi V, Siri JN, Nilsen K, Aquino C, Himmelbach A, Copetti D, Ban T, Venturini L, Bevan M, Clavijo B, Koo DH, Ens J, Wiebe K, N’Diaye A, Fritz AK, Gutwin C, Fiebig A, Fosker C, Fu BX, Accinelli GG, Gardner KA, Fradgley N, Gutierrez-Gonzalez J, Halstead-Nussloch G, Hatakeyama M, Koh CS, Deek J, Costamagna AC, Fobert P, Heavens D, Kanamori H, Kawaura K, Kobayashi F, Krasileva K, Kuo T, McKenzie N, Murata K, Nabeka Y, Paape T, Padmarasu S, Percival-Alwyn L, Kagale S, Scholz U, Sese J, Juliana P, Singh R, Shimizu-Inatsugi R, Swarbreck D, Cockram J, Budak H, Tameshige T, Tanaka T, Tsuji H, Wright J, Wu J, Steuernagel B, Small I, Cloutier S, Keeble-Gagnère G, Muehlbauer G, Tibbets J, Nasuda S, Melonek J, Hucl PJ, Sharpe AG, Clark M, Legg E, Bharti A, Langridge P, Hall A, Uauy C, Mascher M, Krattinger SG, Handa H, Shimizu KK, Distelfeld A, Chalmers K, Keller B, Mayer KFX, Poland J, Stein N, McCartney CA, Spannagl M, Wicker T, Pozniak CJ (2020) Multiple wheat genomes reveal global variation in modern breeding. Nature 588:277–283
Xue F, Guo J, Guan C, Wang H, Li A, Kong L (2015) Molecular mapping of the hybrid necrosis gene NetJingY176 in Aegilops tauschii using microsatellite markers. Crop J 3:298–304
Zeven AC (1972) Determination of the chromosome and its arm carrying the Nel-locus of Triticum aestivum L., Chinese Spring and the Nel-expressivity. Wheat Inform Serv 33:4–6
Zhang P, Hiebert CW, McIntosh RA, McCallum BD, Thomas JB, Hoxha S, Singh D, Bansal U (2016) The relationship of leaf rust resistance gene Lr13 and hybrid necrosis gene Ne2m on wheat chromosome 2BS. Theor Appl Genet 129:485–493
Acknowledgements
This work was partially supported by the National Natural Science Foundation of China (32072063, 31930081, 32000411) and Jiangsu collaborative innovation initiative for modern crop production.
Funding
National Natural Science Foundation of China (32072063, 31930081, 32000411) and Jiangsu collaborative innovation initiative for modern crop production supported this study.
Author information
Authors and Affiliations
Contributions
NL and QYT conducted population construction, phenotyping, genotyping, data analysis, NL prepared the draft; JHD participated in population construction or genotyping, XLP provided the parental lines and contributed to project implementation, ZQM designed the project and reviewed the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflicts of interest.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Xianchun Xia.
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
Li, N., Tan, Q., Ding, J. et al. Fine mapping of Ne1, the hybrid necrosis gene complementary to Ne2 in common wheat (Triticum aestivum L.). Theor Appl Genet 134, 2813–2821 (2021). https://doi.org/10.1007/s00122-021-03860-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-021-03860-9