Novel Cytonuclear Combinations Modify Arabidopsis thaliana Seed Physiology and Vigor.

Clément Boussardon,Benjamin Vittrant,Béatrice Godin,Loïc Rajjou,Françoise Budar,Sylvie Citerne,David Macherel,Marie-Laure Martin-Magniette,Tristan Mary-Huard,Abdelilah Benamar

doi:10.3389/fpls.2019.00032

Abstract

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.

Highlights

The evolutionary success of angiosperms is largely due to the invention of seeds, which protect and scatter the generation and provide it with resources upon germination
In a study using Arabidopsis cytolines, each combining the nuclear genome of a natural variant with the cytoplasmic genomes of a different variant, we previously demonstrated the impact of cytoplasmic natural variation and cytonuclear interactions on adaptive traits in the field, including germination (Roux et al, 2016)
Results were analyzed independently for each PH time and considering both germination temperatures in order to better control the variability of germination success, except for 0PH whose only results at 15◦C were considered because none of the genotypes germinated at 25◦C upon harvest

Summary

Introduction

The evolutionary success of angiosperms is largely due to the invention of seeds, which protect and scatter the generation and provide it with resources upon germination. Dormancy allows the seed to await for the favorable season for seedling success (Finch-Savage and Footitt, 2017). Germination is a trait of primary interest for agriculture, where seed vigor, defined as the properties that ensure a fast and synchronized germination in field conditions (Finch-Savage and Bassel, 2016), is crucial for the quality of seed lots. In the laboratory, seed vigor is assessed through the speed and uniformity of germination in favorable conditions, germination performance under stress conditions, and the ability to survive storage (Finch-Savage et al, 2010; Rajjou et al, 2012). I.e., ability to survive and maintain germination performance despite physiological damage occurring during storage, is an important component of seed vigor (Rajjou and Debeaujon, 2008; Sano et al, 2016)

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Results

Conclusion