Diverse paths to hybrid incompatibility in Arabidopsis

Vaid, Neha; Laitinen, Roosa A. E.

doi:10.1111/tpj.14061

Cited by 26 publications

(28 citation statements)

References 140 publications

(203 reference statements)

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“…Being able to predict hybrid performance -both whether hybrids are better or worse than their parents -is highly valuable in plant breeding. While heterosis or hybrid vigor are desirable, hybrid weakness, with hybrid necrosis being one prominent example among many [12,64], must be avoided. Most, but not all, previously identified hybrid necrosis loci in A. thaliana seem rare [20,22,65].…”

Section: Discussionmentioning

confidence: 99%

“…Conversely, the combination of divergent germplasm, which is an important source of novel variation in breeding, also incurs the risk of genetic incompatibilities. In plants, a particularly conspicuous set of incompatibilities is associated with autoimmunity, often with substantial negative effects on hybrid fitness [11][12][13]. Studies of hybrid autoimmunity in several species, often expressed as hybrid necrosis, have revealed that the underlying genetics tends to be simple, with often only one or two causal loci.…”

Section: Introductionmentioning

confidence: 99%

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RPW8/HR Repeats Predict NLR-dependent Hybrid Performance

Barragan

et al. 2019

Preprint

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Keywords RPW8, NLR, natural variation, autoimmunity, hybrid performance, MLKL, HET-S Barragan et al. RPW8/HR repeats and hybrid necrosis 2 SummaryHybrid offspring can look very different from their parents, including having greatly increased or decreased fitness. In many plant species, conflicts between divergent elements of the immune system can cause hybrids to express autoimmunity, a generally deleterious syndrome known as hybrid necrosis. We are investigating multiple hybrid necrosis cases in Arabidopsis thaliana that are caused by allele-specific interactions between different variants at two unlinked resistance (R) gene clusters. One is the RESISTANCE TO PERONOSPORA PARASITICA 7 (RPP7) cluster, which encodes an intracellular nucleotide binding site-leucine rich repeat (NLR) immune receptors that confer strain-specific resistance to oomycetes. The other is the RESISTANCE TO POWDERY MILDEW 8 (RPW8)/HOMOLOG OF RPW8 (HR) locus, which encodes atypical resistance proteins that can confer broad-spectrum resistance to filamentous pathogens. There is extensive structural variation in the RPW8/HR cluster, both at the level of gene copy number and at the level of C-terminal protein repeats of unknown function. We demonstrate that the number of RPW8/HR repeats correlate, albeit in a complex manner, with the severity of hybrid necrosis when these alleles are combined with specific RPP7 variants. This observation suggests that gross structural differences, rather than individual amino acid polymorphisms, guide the genetic interaction between RPW8/HR and RPP7 alleles. We discuss these findings in light of the similarity of RPW8/HR proteins with pore-forming toxins, MLKL and HET-S, from mammals and fungi.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

RPW8/HR Repeats Predict NLR-dependent Hybrid Performance

Barragan

et al. 2019

Preprint

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“…Since the consequences of inappropriate activation are so profound, it seems likely that NLRs and the proteins that regulate their activity co‐evolve and that divergence of these proteins may occur within subpopulations of a species with low population gene flow. Within the genus Arabidopsis , the progeny of some crosses between species, or between distant accessions within a species, grow poorly and display a necrotic leaf phenotype (Chae et al , ; Vaid and Laitinen, ). In a number of these cases of so‐called hybrid necrosis, the causal genes are NLRs, one from each parent (Bomblies and Weigel, ).…”

Section: Consequencesmentioning

confidence: 99%

The plant hypersensitive response: concepts, control and consequences

Balint‐Kurti

2019

Molecular Plant Pathology

456

277

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Summary The hypersensitive defence response is found in all higher plants and is characterized by a rapid cell death at the point of pathogen ingress. It is usually associated with pathogen resistance, though, in specific situations, it may have other consequences such as pathogen susceptibility, growth retardation and, over evolutionary timescales, speciation. Due to the potentially severe costs of inappropriate activation, plants employ multiple mechanisms to suppress inappropriate activation of HR and to constrain it after activation. The ubiquity of this response among higher plants despite its costs suggests that it is an extremely effective component of the plant immune system.

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“…Post-zygotic, genetic isolation is thought to occur due to epistatic interaction between loci, where alleles arise and fix in allopatry prior to secondary contact, e.g., the Bateson-Dobzhansky-Muller (BDM) model (Bateson, 1909;Dobzhansky, 1936;Muller, 1942). However, many incompatibilities uncovered using high-throughput molecular analyses (Castillo and Barbash, 2017;Kuzmin et al, 2018;Schumer et al, 2018;Vaid and Laitinen, 2019) and quantitative trait locus (QTL) mapping (Moyle and Nakazato, 2008;Turner et al, 2014;Chae et al, 2014;Lowry et al, 2015;Wang et al, 2015), do not conform to the processes assumed by the BDM model. In particular, in both natural populations and model organisms, studies have found that reproductive barriers often exist between allopatric populations experiencing similar selection pressures and that many of the alleles underlying genetic incompatibility predate the allopatric separation of populations (Schluter, 2009;Han et al, 2017;Guerrero and Hahn, 2017;Marques et al, 2019;Jamie and Meier, 2020).…”

Section: Introductionmentioning

confidence: 99%

Reproductive barriers as a byproduct of gene network evolution

Yang

Scarpino

2020

Preprint

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Molecular analyses of closely related taxa have increasingly revealed the importance of 10 higher-order genetic interactions in explaining the observed pattern of reproductive isolation 11 between populations. Indeed, both empirical and theoretical studies have linked the process of 12 speciation to complex genetic interactions. Gene Regulatory Networks (GRNs) capture the 13 inter-dependencies of gene expression and encode information about an individual's phenotype 14 and development at the molecular level. As a result, GRNs can-in principle-evolve via natural 15 selection and play a role in non-selective, evolutionary forces. Here, we develop a network-based 16 model, termed the pathway framework, that considers GRNs as a functional representation of 17 coding sequences. We then simulated the dynamics of GRNs using a simple model that included 18 natural selection, genetic drift, and sexual reproduction and found that reproductive barriers can 19 develop rapidly between allopatric populations experiencing identical selection pressure. Further, 20 we show that alleles involved in reproductive isolation can predate the allopatric separation of 21 populations and that the number of interacting loci involved in genetic incompatibilities, i.e., the 22 order, is often high simply as a by-product of the networked structure of GRNs. Finally, we discuss 23 how results from the pathway framework are consistent with observed empirical patterns for 24 genes putatively involved in post-zygotic isolation. Taken together, this study adds support for the 25 central role of gene networks in speciation and in evolution more broadly. 26 27 31Through this work, it is widely accepted that divergent selection on de novo mutations in geo-32 graphically isolated populations can facilitate speciation, as originally theorized by (Bateson, 1909; 33 Dobzhansky, 1936; Muller, 1942). Despite well-established examples from Drosophila (Brideau34 et al., 2006), Xiphophorus (Wittbrodt et al., 1989; Powell et al., 2020), Oryza (Yamamoto et al., 35 2010), Arabidopsis (Bikard et al., 2009), and Mus (Davies et al., 2016), the genetics and evolutionary 36 history of incompatibilities are typically far more complex and/or less well understood than what 37 is suggested by classical models (Noor and Feder, 2006; Lowry et al., 2008; Presgraves, 2010; Wolf 38 et al., 2010; Nosil and Schluter, 2011; Seehausen et al., 2014; Marques et al., 2019; Dagilis and 39Matute, 2020). 40 Post-zygotic, genetic isolation is thought to occur due to epistatic interaction between loci, where 41 alleles arise and fix in allopatry prior to secondary contact, e.g., the Bateson-Dobzhansky-Muller 42 1 of 26 Manuscript submitted to eLife (BDM) model (Bateson, 1909; Dobzhansky, 1936; Muller, 1942). However, many incompatibilities 43 uncovered using high-throughput molecular analyses (Castillo and Barbash, 2017; Kuzmin et al., 44 2018; Vaid and Laitinen, 2019) and quantitative trait locus (QTL) mapping (Moyle and Nakazato, 45 2008; Turner et al., 2014; Ch...

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Diverse paths to hybrid incompatibility in Arabidopsis

Cited by 26 publications

References 140 publications

RPW8/HR Repeats Predict NLR-dependent Hybrid Performance

RPW8/HR Repeats Predict NLR-dependent Hybrid Performance

The plant hypersensitive response: concepts, control and consequences

Reproductive barriers as a byproduct of gene network evolution

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