Origin of Plant Hybrid Incompatibility

Chen Chen, Yangzhou University, Yangzhou, China

Published online: February 2019

DOI: 10.1002/9780470015902.a0028283

Abstract

Hybrid incompatibility (HI) can cause inviability or sterility of inter‐ or intra‐species hybrids, which hinders gene flow between populations and thus contributes to speciation. HI clearly reduces fitness, but is extremely common across kingdoms. The classic Bateson–Dobzhansky–Muller model suggests that HI is caused by the genic conflicts between independently evolved loci. In this case, HI is simply a by‐product of evolution and has never been selected against. This model is supported by dozens of empirical studies and many incompatible HI‐causal genes have been cloned in recent decades. The HI‐causal genes are usually hyper‐polymorphic and evolve rapidly. Genetic drift, selection and the coevolution of plants with external microbes, or with internal selfish elements, may have driven the evolution of HI. These findings greatly broaden our understanding of the origin of HI.

Key Concepts

  • Hybrid incompatibility is caused by the deleterious interactions between incompatible genes that evolved independently.
  • Hybrid incompatibility is a by‐product of evolution.
  • Co‐evolution of plants and their external or internal factors, such as pathogens and genetic selfish elements, drives the evolution of hybrid incompatibilities in plants.
  • The causal genes of hybrid incompatibilities is predictable.
  • Hybrid incompatibility causal genes are rapidly evolved.
  • Some hybrid incompatibility causal genes are selected.
  • Gene duplication play important roles for the evolution of hybrid incompatibility.

Keywords: hybrid incompatibility; reproductive barriers; Batoson–Dobzhansky–Muller model; HI‐causal gene; evolutionary drive; selection

Figure 1. Illustrations of the extrinsic and intrinsic hybrid incompatibilities. P1 and P2 are individuals from different populations. They showed adaptations to their corresponding environment. For extrinsic hybrid incompatibility (a), the hybrids derived from P1 and P2 cannot survive in the niches of their parents. The failure of the hybrids is due to difficulties to find a suitable ecological niche. In contract, for intrinsic hybrid incompatibilities (b), the inferior hybrids derived from P1 and P2 are caused by internal development defects rather than ecological maladaptation. They cannot survive in any environment.
Figure 2. Understanding of the Bateson–Dobzhansky–Muller model in an evolutionary aspect. The ancestral population have been divided into two distinct populations owing to geographic barriers. The genotype of the ancestor was aa and bb at the loci ‘a’ and ‘b’, respectively. In one population, the ‘a’ allele was mutated into ‘A’ and fixed in the population; while in the other, the ‘b’ allele was evolved into ‘B’ and fixed. The ‘A’ and ‘B’ alleles are not compatible, which cause the inviability or sterility of the hybrids derived from the two populations. Because the alleles ‘A’ and ‘B’ never had chance to be tested in the history, the inferior hybrid do not represent a necessary step for evolution. Instead, they are by‐products of the evolution. Recent studies revealed that some of the causal genes of hybrid incompatibilities were directly selected. In addition, genetic drift and hitchhiking effect may also contribute to the evolution of hybrid incompatibilities.
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References

Alcázar R , García AV , Kronholm I , et al. (2010) Natural variation at Strubbelig Receptor Kinase 3 drives immune‐triggered incompatibilities between Arabidopsis thaliana accessions. Nature Genetics 42: 1135–1139.

Alcázar R , García AV , Parker JE and Reymond M (2009) Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proceedings of the National Academy of Sciences of the United States of America 106: 334–339.

Bayes JJ and Malik HS (2009) Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326: 1538–1541.

Bikard D , Patel D , Le Metté C , et al. (2009) Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana . Science 323: 623–626.

Blevins T , Wang J , Pflieger D , Pontvianne F and Pikaard CS (2017) Hybrid incompatibility caused by an epiallele. Proceedings of the National Academy of Sciences of the United States of America 114: 4–9.

Bomblies K , Lempe J , Epple P , et al. (2007) Autoimmune response as a mechanism for a Dobzhansky‐Muller‐type incompatibility syndrome in plants. PLoS Biology 5: 1962–1972.

Bouche N , Strand EP and Bourgin IJ (2012) Report rapid establishment of genetic incompatibility through natural epigenetic variation. Current Biology 22: 326–331.

Burkart‐Waco D , Josefsson C , Dilkes B , et al. (2012) Hybrid incompatibility in Arabidopsis is determined by a multiple‐locus genetic network. Plant Physiology 158: 801–812.

Case AL , Finseth FR , Barr CM and Fishman L (2016) Selfish evolution of cytonuclear hybrid incompatibility in Mimulus . Proceedings of the Royal Society B: Biological Sciences 283.

Chae E , Bomblies K , Kim S‐T , et al. (2014) Species‐wide genetic incompatibility analysis identifies immune genes as Hot spots of deleterious epistasis. Cell 159: 1341–1351.

Chen C , Chen H , Lin Y‐S , et al. (2014) A two‐locus interaction causes interspecific hybrid weakness in rice. Nature Communications 5: 3357.

Chen C , E and Lin H (2016) Evolution and molecular control of hybrid incompatibility in plants. Frontiers in Plant Science 7: 1208.

Chen L and Liu Y‐G (2014) Male sterility and fertility restoration in crops. Annual Review of Plant Biology 65: 579–606.

Chu Y and Oka H (1970) The genetic basis of crossing barriers between Oryza perennis subsp. barthii and its related taxa. Evolution 24: 135–144.

Coyne JA and Orr HA (2004) Speciation. Sunderland, MA: Sinauer Associates.

Cui X , Wise RP and Schnable PS (1996) The rf2 nuclear restorer gene of male‐sterile T‐cytoplasm maize. Science 272: 1334–1336.

Duxbury Z , Ma Y , Furzer OJ , et al. (2016) Pathogen perception by NLRs in plants and animals: parallel worlds. BioEssays 38: 769–781.

Fishman L and Sweigart AL (2018) When two rights make a wrong: the evolutionary genetic of plant hybrid incompatabilities. Annual Review of Plant Biology 69: 1–25.

Florez‐Rueda AM , Paris M , Schmidt A , et al. (2016) Genomic imprinting in the endosperm is systematically perturbed in abortive hybrid tomato seeds. Molecular Biology and Evolution 33: 2935–2946.

Fujii S and Toriyama K (2009) Suppressed expression of RETROGRADE‐REGULATED MALE STERILITY restores pollen fertility in cytoplasmic male sterile rice plants. Proceedings of the National Academy of Sciences 106: 9513–9518.

Garner AG , Kenney AM , Fishman L and Sweigart AL (2016) Genetic loci with parent of origin effects cause hybrid seed lethality between Mimulus species. New Phytologist 211: 319–331.

Haig D and Westoby M (1991) Genomic imprinting in endosperm: its effect on seed development in crosses between species, and between different ploidies of the same species, and its implications for the evolution of apomixis. Philosophical Transactions of the Royal Society, B: Biological Sciences 333: 1–13.

Ichitani K , Takemoto Y , Iiyama K , Taura S and Sato M (2012) Chromosomal location of HCA1 and HCA2, hybrid chlorosis genes in rice. International Journal of Plant Genomics 2012: 1–9.

Jeuken MJW , Zhang NW , McHale LK , et al. (2009) Rin4 causes hybrid necrosis and race‐specific resistance in an interspecific lettuce hybrid. The Plant Cell 21: 3368–3378.

Josefsson C , Dilkes B and Comai L (2006) Parent‐dependent loss of gene silencing during interspecies hybridization. Current Biology 16: 1322–1328.

Kirkbride RC , Yu HH , Nah G , et al. (2015) An epigenetic role for disrupted paternal gene expression in postzygotic seed abortion in Arabidopsis interspecific hybrids. Molecular Plant 8: 1766–1775.

Kradolfer D , Wolff P , Jiang H , Siretskiy A and Kohler C (2013) An imprinted gene underlies postzygotic reproductive isolation in Arabidopsis thaliana . Developmental Cell 26: 525–535.

Lafon‐Placette C , Johannessen IM , Hornslien KS , et al. (2017) Endosperm‐based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe. Proceedings of the National Academy of Sciences of the United States of America 114: E1027–E1035.

Mizuta Y , Harushima Y and Kurata N (2010) Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proceedings of the National Academy of Sciences of the United States of America 107: 20417–20422.

Nguyen GN , Yamagata Y , Shigematsu Y , Watanabe M and Miyazaki Y (2017) Duplication and loss of function of genes encoding RNA polymerase III subunit C4 causes hybrid incompatibility in rice. Genes, Genomes, Genetics G3 7: 2565–2575.

Orr HA (1996) Dobzhansky, Bateson, and the genetics of speciation. Genetics 144: 1331–1335.

Pires ND and Grossniklaus U (2014) Different yet similar: evolution of imprinting in flowering plants and mammals. F1000prime Reports 6: 63.

Plötner B , Nurmi M , Fischer A , et al. (2017) Chlorosis caused by two recessively interacting genes reveals a role of RNA helicase in hybrid breakdown in Arabidopsis thaliana . Plant Journal 91: 251–262.

Presgraves DC (2010) The molecular evolutionary basis of species formation. Nature Reviews Genetics 11: 175–180.

Pukhalskiy VA , Martynov SP and Dobrotvorskaya TV (2000) Analysis of geographical and breeding‐related distribution of hybrid necrosis genes in bread wheat (Triticum aestivum L.). Euphytica 114: 233–240.

Rieseberg LH and Blackman BK (2010) Speciation genes in plants. Annals of Botany 106: 439–455.

Sekine D , Ohnishi T , Furuumi H , et al. (2013) Dissection of two major components of the post‐zygotic hybridization barrier in rice endosperm. The Plant Journal: For Cell and Molecular Biology 76: 792–799.

Shen R , Wang L , Liu X , et al. (2017) Genomic structural variation‐mediated allelic suppression causes hybrid male sterility in rice. Nature Communications 8: 1310.

Sicard A , Kappel C , Josephs EB , et al. (2015) Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene‐flow barriers in Capsella . Nature Communications 6: 7960.

Sweigart AL , Fishman L and Willis JH (2006) A simple genetic incompatibility causes hybrid male sterility in Mimulus . Genetics 172: 2465–2479.

Sweigart AL and Flagel LE (2015) Evidence of natural selection acting on a polymorphic hybrid incompatibility locus in Mimulus . Genetics 199: 543–554.

Swiadek M , Proost S , Sieh D , et al. (2017) Novel allelic variants in ACD6 cause hybrid necrosis in local collection of Arabidopsis thaliana . New Phytologist 213: 900–915.

Tang H , Zheng X , Li C , et al. (2017) Multi‐step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes. Cell Research 27: 130–146.

Todesco M , Kim ST , Chae E , et al. (2014) Activation of the Arabidopsis thaliana immune system by combinations of common ACD6 alleles. PLoS Genetics 10: e1004459.

Wang P , Bai W , Zheng H , et al. (2018) A selfish genetic element confers non‐Mendelian inheritance in rice. Science 360: 1130–1132.

Wolff P , Jiang H , Wang G , Santos‐González J and Köhler C (2015) Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana . eLife 4: 1–14.

Wright KM , Lloyd D , Lowry DB , Macnair MR and Willis JH (2013) Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus . PLoS Biology 11: e1001497.

Yamagata Y , Yamamoto E , Aya K , et al. (2010) Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Proceedings of the National Academy of Sciences of the United States of America 107: 1494–1499.

Yang J , Zhao X , Cheng K , et al. (2012) A killer‐protector system regulates both hybrid sterility and segregation distortion in rice. Science 337: 1336–1340.

Zuellig MP and Sweigart AL (2018) Gene duplicates cause hybrid lethality between sympatric species of Mimulus . PLoS Genetics 14: 1–20.

Further Reading

Baack E , Melo MC , Rieseberg LH and Ortiz‐Barrientos D (2015) The origins of reproductive isolation in plants. New Phytologist 207: 968–984.

Bomblies K and Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene‐flow barrier in plant species. Nature Reviews Genetics 8: 382–393.

Dempewolf H , Hodgins KA , Rummell SE , Ellstrand NC and Rieseberg LH (2012) Reproductive isolation during domestication. The Plant Cell 24: 2710–2717.

Lafon‐Placette C , Vallejo‐Marín M , Parisod C , Abbott RJ and Köhler C (2016) Current plant speciation research: unravelling the processes and mechanisms behind the evolution of reproductive isolation barriers. The New Phytologist 209: 29–33.

Maheshwari S and Barbash D (2011) The genetics of hybrid incompatibilities. Annual Review of Genetics 45: 331–355.

Ouyang Y and Zhang Q (2013) Understanding reproductive isolation based on the rice model. Annual Review of Plant Biology 64: 111–135.

Vaid N and Laitinen RAE (2018) Diverse paths to hybrid incompatibility in Arabidopsis . The Plant Journal: 1–15.

Related Sub-Topics:

Plant Evolution | Plant Genetics and Molecular Biology | Evolution: Theories and Ideas | Evolutionary Processes | Population Structure and Genetics | Evolution of Species
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Article Title: Origin of Plant Hybrid Incompatibility
 
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Chen, Chen(Feb 2019) Origin of Plant Hybrid Incompatibility. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028283]