Gene expression and genetic divergence in oak species highlight adaptive genes to soil water constraints

Author:

Le Provost Grégoire1ORCID,Brachi Benjamin1ORCID,Lesur Isabelle12ORCID,Lalanne Céline1ORCID,Labadie Karine3ORCID,Aury Jean-Marc4ORCID,Da Silva Corinne4ORCID,Postolache Dragos5ORCID,Leroy Thibault16ORCID,Plomion Christophe1ORCID

Affiliation:

1. INRAE, Univ. Bordeaux, BIOGECO , Cestas, F-33610, France

2. Helix Venture , Mérignac, F-33700, France

3. Genoscope, Institut de Biologie François-Jacob, Commissariat à l'Energie Atomique (CEA), Université Paris-Saclay , Evry, 91057, France

4. Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay , Evry, 91057, France

5. National Institute for Research and Development in Forestry “Marin Drăcea”, Cluj Napoca Research Station , Cluj-Napoca, 400202, Romania

6. IRHS-UMR1345, Université d’Angers, INRAE, Institut Agro , Beaucouzé, 49071, France

Abstract

Abstract Drought and waterlogging impede tree growth and may even lead to tree death. Oaks, an emblematic group of tree species, have evolved a range of adaptations to cope with these constraints. The two most widely distributed European species, pedunculate (PO; Quercus robur L.) and sessile oak (SO; Quercus petraea Matt. Lieb), have overlapping ranges, but their respective distribution are highly constrained by local soil conditions. These contrasting ecological preferences between two closely related and frequently hybridizing species constitute a powerful model to explore the functional bases of the adaptive responses in oak. We exposed oak seedlings to waterlogging and drought, conditions typically encountered by the two species in their respective habitats, and studied changes in gene expression in roots using RNA-seq. We identified genes that change in expression between treatments differentially depending on species. These “species × environment”-responsive genes revealed adaptive molecular strategies involving adventitious and lateral root formation, aerenchyma formation in PO, and osmoregulation and ABA regulation in SO. With this experimental design, we also identified genes with different expression between species independently of water conditions imposed. Surprisingly, this category included genes with functions consistent with a role in intrinsic reproductive barriers. Finally, we compared our findings with those for a genome scan of species divergence and found that the expressional candidate genes included numerous highly differentiated genetic markers between the two species. By combining transcriptomic analysis, gene annotation, pathway analyses, as well as genome scan for genetic differentiation among species, we were able to highlight loci likely involved in adaptation of the two species to their respective ecological niches.

Funder

INRAE

European Union’s

Publisher

Oxford University Press (OUP)

Subject

Plant Science,Genetics,Physiology

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