The hybrid lethality of interspecific F1 hybrids of Nicotiana: a clue to understanding hybrid inviability—a major obstacle to wide hybridization and introgression breeding of plants

Self Cite

Enhanced ovary abscission after pollination and hybrid seed lethality result in post-zygotic reproductive isolation in plant interspecific crosses. However, the connection between these barriers remains unclear. Here, we report that an imbalance in parental genomes or endosperm balance number (EBN) causes hybrid seed lethality and ovary abscission in both interspecific and intraspecific-interploidy crosses in the genus Nicotiana. Auxin treatment suppressed ovary abscission, but not hybrid seed lethality, in an interspecific cross between Nicotiana suaveolens and N. tabacum, suggesting that ovary abscission-related genes are located downstream of those involved in hybrid seed lethality. We performed interploidy crosses among N. suaveolens tetraploids, octoploids, and neopolyploids and revealed hybrid seed lethality and ovary abscission in interploid crosses. Furthermore, a higher maternal EBN than paternal EBN caused these barriers, as previously observed in N. suaveolens × N. tabacum crosses. Altogether, these results suggest that maternal excess of EBN causes hybrid seed lethality, which in turn leads to ovary abscission through the same mechanism in both interspecific and interploidy crosses.

Section: Introductionmentioning

confidence: 99%

Parental Genome Imbalance Causes Hybrid Seed Lethality as Well as Ovary Abscission in Interspecific and Interploidy Crosses in Nicotiana

Sadahisa

Yokoi

et al. 2022

Self Cite

“…These findings suggest the involvement of HSP90-SGT1-RAR1 complex in type II hybrid seedling lethality. Because each species has established an appropriate set of chaperons, the chaperons may be incompatible with those from other species ( Katsuyama et al., 2021 ; Mino et al., 2022 ).…”

Section: Hybrid Seedling Lethalitymentioning

confidence: 99%

“…Ecogeographic isolation and pollinator isolation (pollinator fidelity in a natural mixed population) are typical examples of pre-mating isolation barriers ( Ramsey et al., 2003 ; Coyne and Orr, 2004 ; Savolainen et al., 2006 ; Streisfeld and Kohn, 2007 ; Zhang et al., 2022a ), whereas interspecific pollen-pistil incompatibility, conspecific pollen precedence, gametic incompatibility, and pistil-length mismatch are examples of post-mating prezygotic isolating barriers ( Rieseberg and Willis, 2007 ; Lee et al., 2008 ; Rieseberg and Blackman, 2010 ; Huang et al., 2023 ). Postzygotic isolation barriers include hybrid seed lethality ( Bikard et al., 2009 ; Dziasek et al., 2021 ), immature fruit abscission ( Gupta et al., 1996 ; He et al., 2019 ; Kawaguchi et al., 2021 ), hybrid seedling lethality or inviability ( Tezuka et al., 2010 ; Tezuka, 2013 ; Xiao et al., 2017 ; Deng et al., 2019 ; Mino et al., 2022 ), hybrid weakness ( Ichitani et al., 2011 ; Shiragaki et al., 2020b ), hybrid sterility ( Yamagata et al., 2010 ; Koide et al., 2018 ; Li et al., 2020 ), and hybrid breakdown ( Li et al., 1997 ; Kubo and Yoshimura, 2005 ; Zhang et al., 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Understanding and overcoming hybrid lethality in seed and seedling stages as barriers to hybridization and gene flow

Shiragaki

Tezuka³

2023

Self Cite

Hybrid lethality is a type of reproductive isolation barrier observed in two developmental stages, hybrid embryos (hybrid seeds) and hybrid seedlings. Hybrid lethality has been reported in many plant species and limits distant hybridization breeding including interspecific and intergeneric hybridization, which increases genetic diversity and contributes to produce new germplasm for agricultural purposes. Recent studies have provided molecular and genetic evidence suggesting that underlying causes of hybrid lethality involve epistatic interaction of one or more loci, as hypothesized by the Bateson–Dobzhansky–Muller model, and effective ploidy or endosperm balance number. In this review, we focus on the similarities and differences between hybrid seed lethality and hybrid seedling lethality, as well as methods of recovering seed/seedling activity to circumvent hybrid lethality. Current knowledge summarized in our article will provides new insights into the mechanisms of hybrid lethality and effective methods for circumventing hybrid lethality.

“…Carolus Linnaeus proposed a radical evolutionary hypothesis that new species could arise via hybridization ( Larson, 1968 ). Interspecific hybridization occurred or is carried out in many plants ( Kopecký et al, 2022 ), such as tomato ( Lippman et al, 2007 ), cotton ( Zhang et al, 2014 ), soybean ( Wang et al, 2019 ), rice ( Purugganan, 2019 ), grape ( Foria et al, 2022 ), tobacco ( Mino et al, 2022 ), and oak ( Fu et al, 2022 ), served as an important mechanism for their genetic diversification, environment adaptation, and range expansion, as well as improvement of economical traits. Older crops, such as rice, also have longer time to diversify under cultivation and thus adapt to local environments as their geographic ranges widened ( Milla and Osborne, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Interspecific Hybridization Is an Important Driving Force for Origin and Diversification of Asian Cultivated Rice Oryza sativa L.

Zhou

Yang

et al. 2022

As one of the most important crops, Asian cultivated rice has evolved into a complex group including several subgroups adapting various eco-climate-systems around the globe. Here, we pictured a comprehensive view of its original domestication, divergences, and the origin of different subgroups by integrating agriculture, archeology, genetics, nuclear, and cytoplasm genome results. Then, it was highlighted that interspecific hybridization-introgression has played important role in improving the genetic diversity and adaptation of Oryza sativa during its evolution process. Natural hybridization-introgression led to the origin of indica, aus, and basmatic subgroups, which adapted to changing cultivated environments, and produced feral weedy rice coexisting and competing with cultivars under production management. Artificial interspecific hybridization-introgression gained several breakthroughs in rice breeding, such as developing three-line hybrid rice, new rice for Africa (NERICA), and some important pest and disease resistance genes in rice genetic improvement, contributing to the stable increase of rice production to meet the expanding human population. We proposed a series to exploit the virtues of hybridization-introgression in the genetic improvement of Asian cultivated rice. But some key issues such as reproductive barriers especially hybrid sterility should be investigated further, which are conducive to gene exchange between cultivated rice and its relatives, and even is beneficial to exploiting interspecific hybrid vigor. New technologies help introduce favorable genes from distant wild species to Asian cultivated rice, such as transgenic and genome editing systems. Rising introgression lines in a wider range with multi-donor benefits allele mining, understanding genetic network of rice growth and development, yield formation, and environmental adaptation. Then, integration of new tools and interspecific hybridization can be a future direction to develop more usable breeding populations which can make Asian cultivated rice more resilient to the changing climate and world.