Natural variation at Strubbelig Receptor Kinase 3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions

Alcázar, Rubén; García, Ana Victoria Torres; Kronholm, Ilkka; Meaux, Juliette de; Koornneef, M.; Parker, Jane E.; Reymond, Matthieu

doi:10.1038/ng.704

Cited by 121 publications

(138 citation statements)

References 34 publications

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“…Finally, the pseudooverdominance hypothesis also explains heterosis with the complementation of recessive alleles but proposes that when linked in repulsion, such alleles appear overdominant. Outside of these classical hypotheses, some cases of hybrid inferiority (19)(20)(21)(22) and hybrid superiority (23-30) have been linked to epistatic interactions between parental alleles.The availability of completely homozygous natural accessions has made the model plant Arabidopsis thaliana an excellent subject for studies of natural variation. Collections of sequenced accessions enable replicated genome-wide association (GWA)…”

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Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Seymour

Chae

Grimm

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The ubiquity of nonparental hybrid phenotypes, such as hybrid vigor and hybrid inferiority, has interested biologists for over a century and is of considerable agricultural importance. Although examples of both phenomena have been subject to intense investigation, no general model for the molecular basis of nonadditive genetic variance has emerged, and prediction of hybrid phenotypes from parental information continues to be a challenge. Here we explore the genetics of hybrid phenotype in 435 Arabidopsis thaliana individuals derived from intercrosses of 30 parents in a half diallel mating scheme. We find that nonadditive genetic effects are a major component of genetic variation in this population and that the genetic basis of hybrid phenotype can be mapped using genome-wide association (GWA) techniques. Significant loci together can explain as much as 20% of phenotypic variation in the surveyed population and include examples that have both classical dominant and overdominant effects. One candidate region inherited dominantly in the half diallel contains the gene for the MADS-box transcription factor AGAMOUS-LIKE 50 (AGL50), which we show directly to alter flowering time in the predicted manner. Our study not only illustrates the promise of GWA approaches to dissect the genetic architecture underpinning hybrid performance but also demonstrates the contribution of classical dominance to genetic variance.T he often observed phenotypic superiority of progeny relative to their parents, or heterosis, is a universal phenomenon and of great importance to plant agriculture. The earliest description of heterosis (also known as hybrid vigor or superiority) dates to Darwin's studies of cross-fertilization in plants. He noticed that intercrossing distantly related individuals gave rise to larger, more vigorous progeny (1). Four decades later, George Shull coined the term "heterosis" (2) for this phenomenon, which he and Edward East had independently described for hybrids of inbred maize in 1908 (3, 4). Heterosis has long been of interest to evolutionary biologists as a potential explanation for the ubiquity of cross-fertilization in plants and animals, but it is also a central component of agricultural breeding programs. The combination of hybrid seed technology and inbred line improvement has driven an unprecedented improvement in maize yield over the past century (5). Despite the economic importance of heterosis and its intensive investigation in a wide spectrum of species, prediction of hybrid performance from parental information remains a major challenge (6).In the terms of quantitative genetics, hybrid vigor (and its opposite, inferiority) describes a deviation of progeny from the phenotypic mean of the parents. This means that heterosis cannot be explained by the addition of the effects of contributing alleles (7). Nonadditive genetic variance can result from a nonlinear phenotypic effect of alleles at one locus, as in the case of dominant/recessive allele pairs in classical genetics, or from epistatic interactions ...

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Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Seymour

Chae

Grimm

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…tauschii. Disease resistance genes encoding NB-LRR-type resistance (R) proteins and R-interacting proteins have been identified as causal genes for hybrid incompatibilities such as hybrid necrosis in higher plants Alcázar et al, 2009Alcázar et al, , 2010Yamamoto et al, 2010;Chen et al, 2013). Among the 33 Ae.…”

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“…Another Hch gene, Hch2, complementary to Hch1 is proposed to be present in the AB genome of tetraploid wheat, but no information on it or its chromosome location has been reported. In hybrid necrosis of higher plants, most causal genes that have been isolated to date are related to disease resistance Alcázar et al, 2009Alcázar et al, , 2010Yamamoto et al, 2010). In our previous study, comparative transcriptome analyses showed that up-regulation of defense-and carbohydrate metabolism-related genes is common in hybrid chlorosis and type III necrosis, suggesting the existence of common mechanisms that induce their symptoms (Nakano et al, 2015).…”

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Fine mapping of <i>Hch1</i>, the causal D-genome gene for hybrid chlorosis in interspecific crosses between tetraploid wheat and <i>Aegilops tauschii</i>

et al. 2015

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Hybrid chlorosis, one of the reproductive barriers between tetraploid wheat and its D-genome progenitor, Aegilops tauschii, inhibits normal growth of synthetic wheat hexaploids. Hybrid chlorosis appears to be due to an epistatic interaction of two loci from the AB and D wheat genomes. Our previous study assigned the causal D-genome gene for hybrid chlorosis, Hch1, to the short arm of chromosome 7D. Here, we constructed a fine map of 7DS near Hch1 using 280 F 2 individuals from a cross of two wheat synthetic lines, one showing normal growth and the other showing hybrid chlorosis. The hybrid chlorosis phenotype was controlled by a single dominant allele of the Hch1 locus in the synthetic hexaploids. Hch1 was closely linked to four new markers within 0.2 cM, and may be localized near or within the two Ae. tauschii scaffolds containing the linked markers on 7DS. Comparative analysis of the Hch1 chromosomal region for Ae. tauschii, barley and Brachypodium showed that a local inversion occurred in the region proximal to Hch1 during the divergence between barley and Ae. tauschii, and that the Hch1 region on wheat 7DS is syntenic to Brachypodium chromosome 1. These observations provide useful information for further studies toward map-based cloning of Hch1.

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“…Recent reports showed that the causal genes for hybrid necrosis are defense response-related genes in higher plants such as Arabidopsis and lettuce. [13][14][15][16] These hybrid necrosis genes act to accelerate genetic differentiation among genetically related accessions in the same species and between hybrid necrosis sometimes appears in triploid hybrids between tetraploid wheat and Aegilops tauschii Coss. two types of hybrid necrosis (type ii and type iii) were observed when cultivar Langdon was used as female parent for hybrid production.…”

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Low temperature-induced necrosis shows phenotypic plasticity in wheat triploid hybrids

Takumi

Mizuno

2011

Plant Signaling & Behavior

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Common wheat (Triticum aestivum L.) is an allohexaploid species (AABBDD genome), derived through endoreduplication of an interspecific triploid hybrid between cultivated tetraploid wheat Triticum turgidum L. (AABB genome) and a wild diploid relative, Aegilops tauschii Coss (DD genome). Natural hybridization of the parental species, avoidance of hybrid breakdown, and formation of unreduced gametes are essential for hexaploidization. 1The breakdown of wheat triploid hybrids was first reported in Nishikawa's pioneer works.2-4 It was recently found that cultivar Langdon of T. turgidum subspecies durum is an efficient AB genome parent for production of hexaploid wheat synthetics, 5 allowing us to produce a number of synthetic hexaploid wheat lines with D genomes derived from various accessions of Ae. tauschii. 6,7 In the process of synthetic wheat production, we found several types of hybrid abnormalities including hybrid necrosis and hybrid chlorosis, 8,9 as Nishikawa reported previously in references 2-4.Hybrid necrosis is one of the post-zygotic hybridization barriers between two diverging lineages within the same species or in two closely related species. 10 The Dobzhansky-Muller model simply explains the process for generating hybridization barriers. 11,12 In diploid species, post-zygotic hybridization barriers, including hybrid necrosis, function in a positive manner to accelerate establishment of a new diploid species. Recent reports showed that the causal genes for hybrid necrosis are defense response-related genes in higher plants such as Arabidopsis and lettuce. [13][14][15][16] These hybrid necrosis genes act to accelerate genetic differentiation among genetically related accessions in the same species and between hybrid necrosis sometimes appears in triploid hybrids between tetraploid wheat and Aegilops tauschii Coss. two types of hybrid necrosis (type ii and type iii) were observed when cultivar Langdon was used as female parent for hybrid production. type ii necrosis symptoms occurred only under low temperature conditions, whereas bushy and dwarf phenotypes were observed under normal temperature conditions. the developmental plasticity might be related to a temperature-responsive alteration of meristematic activity at the crown tissue of triploid hybrids. Epistatic interaction between the aB and D genomes induced not only upregulation of a number of defense-related genes, but also extensive changes in plant architecture in the type ii necrosis hybrids. Such phenotypic plasticity was also observed in other cross combinations between cultivated tetraploid wheat and type ii necrosis-induced Ae. tauschii accessions. Wild tetraploid wheat, Triticum turgidum subspecies dicoccoides, did not induce type ii necrosis in the triploid hybrids, indicating the possibility of identifying the chromosomal location of a causal gene for type ii necrosis in the aB genome. Low temperature-induced necrosis shows phenotypic plasticity in wheat triploid hybridsShigeo takumi* and nobuyuki mizuno Graduate School of agricultura...

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Natural variation at Strubbelig Receptor Kinase 3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions

Cited by 121 publications

References 34 publications

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Fine mapping of <i>Hch1</i>, the causal D-genome gene for hybrid chlorosis in interspecific crosses between tetraploid wheat and <i>Aegilops tauschii</i>

Low temperature-induced necrosis shows phenotypic plasticity in wheat triploid hybrids

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