Boussardon Clément, Martin-Magniette Marie-Laure, Godin Béatrice, Benamar Abdelilah, Vittrant Benjamin, Citerne Sylvie, Mary-Huard Tristan, Macherel David, Rajjou Loïc, Budar Françoise
Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, Versailles, France.
UMR MIA-Paris, AgroParisTech, Institut National de la Recherche Agronomique, Université Paris-Saclay, Paris, France.
Front Plant Sci. 2019 Feb 5;10:32. doi: 10.3389/fpls.2019.00032. eCollection 2019.
Dormancy and germination vigor are complex traits of primary importance for adaptation and agriculture. Intraspecific variation in cytoplasmic genomes and cytonuclear interactions were previously reported to affect germination in Arabidopsis using novel cytonuclear combinations that disrupt co-adaptation between natural variants of nuclear and cytoplasmic genomes. However, specific aspects of dormancy and germination vigor were not thoroughly explored, nor the parental contributions to the genetic effects. Here, we specifically assessed dormancy, germination performance and longevity of seeds from Arabidopsis plants with natural and new genomic compositions. All three traits were modified by cytonuclear reshuffling. Both depth and release rate of dormancy could be modified by a changing of cytoplasm. Significant changes on dormancy and germination performance due to specific cytonuclear interacting combinations mainly occurred in opposite directions, consistent with the idea that a single physiological consequence of the new genetic combination affected both traits oppositely. However, this was not always the case. Interestingly, the ability of parental accessions to contribute to significant cytonuclear interactions modifying the germination phenotype was different depending on whether they provided the nuclear or cytoplasmic genetic compartment. The observed deleterious effects of novel cytonuclear combinations (in comparison with the nuclear parent) were consistent with a contribution of cytonuclear interactions to germination adaptive phenotypes. More surprisingly, we also observed favorable effects of novel cytonuclear combinations, suggesting suboptimal genetic combinations exist in natural populations for these traits. Reduced sensitivity to exogenous ABA and faster endogenous ABA decay during germination were observed in a novel cytonuclear combination that also exhibited enhanced longevity and better germination performance, compared to its natural nuclear parent. Taken together, our results strongly support that cytoplasmic genomes represent an additional resource of natural variation for breeding seed vigor traits.
休眠和萌发活力是对适应和农业至关重要的复杂性状。先前有报道称，利用破坏核基因组和细胞质基因组自然变体之间协同适应的新型细胞质-细胞核组合，细胞质基因组的种内变异和细胞质-细胞核相互作用会影响拟南芥的萌发。然而，休眠和萌发活力的具体方面并未得到充分探索，亲本对遗传效应的贡献也未明确。在此，我们专门评估了具有自然和新基因组组成的拟南芥植株种子的休眠、萌发表现和寿命。所有这三个性状都因细胞质-细胞核重排而发生了改变。细胞质的变化可以改变休眠的深度和解除速率。由于特定的细胞质-细胞核相互作用组合导致的休眠和萌发表现的显著变化主要发生在相反的方向，这与新遗传组合的单一生理后果对这两个性状产生相反影响的观点一致。然而，情况并非总是如此。有趣的是，亲本种质对改变萌发表型的显著细胞质-细胞核相互作用的贡献能力因它们提供的是核遗传部分还是细胞质遗传部分而有所不同。与核亲本相比，新型细胞质-细胞核组合所观察到的有害效应与细胞质-细胞核相互作用对萌发适应性表型的贡献一致。更令人惊讶的是，我们还观察到新型细胞质-细胞核组合的有利效应，这表明在自然种群中这些性状存在次优的遗传组合。与天然核亲本相比，在一种新型细胞质-细胞核组合中观察到对外源脱落酸的敏感性降低以及萌发期间内源脱落酸更快降解，该组合还表现出延长的寿命和更好的萌发表现。综上所述，我们的结果有力地支持了细胞质基因组是种子活力性状育种中自然变异的额外来源这一观点。
