Non‐functional GoFLA19s are responsible for the male sterility caused by hybrid breakdown in cotton (Gossypium spp.)

Abstract

SUMMARY Hybrid breakdown (HB) functions as a common reproductive barrier and reduces hybrid fitness in many species, including cotton. However, the related genes and the underlying genetic mechanisms of HB in cotton remain unknown. Here, we found that the photosensitive genetic male sterile line CCRI9106 was a hybrid progeny of Gossypium hirsutum and Gossypium barbadense and probably a product of HB. Fine mapping with F2s (CCRI9106 × G. hirsutum/G. barbadense lines) identified a pair of male sterility genes GoFLA19s (encoding fasciclin‐like arabinogalactan family protein) located on chromosomes A12 and D12. Crucial variations occurring in the fasciclin‐like domain and the arabinogalactan protein domain were predicted to cause the non‐functionalization of GbFLA19‐D and GhFLA19‐A. CRISPR/Cas9‐mediated knockout assay confirmed the effects of GhFLA19s on male sterility. Sequence alignment analyses showed that variations in GbFLA19‐D and GhFLA19‐A likely occurred after the formation of allotetraploid cotton species. GoFLA19s are specifically expressed in anthers and contribute to tapetal development, exine assembly, intine formation, and pollen grain maturation. RNA‐sequencing and quantitative reverse transcriptase–polymerase chain reaction analyses illustrated that genes related to these biological processes were significantly downregulated in the mutant. Our research on male sterility genes, GoFLA19s, improves the understanding of the molecular characteristics and evolutionary significance of HB in interspecific hybrid breeding.

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

“…Conspecific pollen precedence and gametic incompatibility are examples of post-mating prezygotic isolating barriers ( Rieseberg and Willis, 2007 ). In turn, postzygotic isolation barriers include enlarged ovary (immature fruit) abscission ( Gupta et al, 1996 ; He et al, 2019 ), seed abortion or hybrid seed lethality ( Coughlan et al, 2020 ; Dziasek et al, 2021 ), hybrid weakness ( Shiragaki et al, 2019 , 2020 ), hybrid lethality ( Kawaguchi et al, 2021 ; Si et al, 2021 ; Tezuka et al, 2021 ; Mino et al, 2022 ), and hybrid sterility ( Li et al, 2020 ) in seedlings of the F 1 generation, as well as hybrid breakdown recognized in generations after the F 1 ( Matsubara et al, 2007 ; Zhang et al, 2021 ). These isolating barriers may be observed independently or combined, even in a single cross-combination.…”

Acetylation of GhCaM7 enhances cotton resistance to Verticillium dahliae

“…HM‐1 as the recipient. Cotton transformation was done according to a protocol previously described (Zhang et al., 2021). The T 3 lines overexpressing pCAMBIA2300‐ GhCaM7 were identified by PCR amplification of the transgene and further confirmed by Western blotting analysis using anti‐HA tag primary monoclonal antibody as described (Liu et al., 2021, Yu et al., 2012).…”

“…GO pathway analysis was performed on DEGs to determine statistically enriched GO terms and pathways ( P < 0.05) (Kanehisa et al., 2008). GO terms and KEGG pathways analysis were identify using Omicshare tools (https://www.omicshare.com/tools/) (Zhang et al., 2021). Venn diagrams were generated using the Omicshare tools (https://www.omicshare.com/tools/).…”

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

“…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 ).…”