A haplotype-resolved reference genome of Quercus alba sheds light on the evolutionary history of oaks

Abstract

Introduction

Oaks (Quercus spp.) are important members of ecosystems throughout much of the world (Kremer & Hipp, 2020). In eastern North America, white oak (Quercus alba) is a keystone species and is one of the most abundant forest trees across much of its range (Rogers, 1990; Fralish, 2004). In addition to its ecological and cultural importance (Abrams, 2003; Bocsi et al., 2021a,b; Stringer & Morris, 2022), white oak has significant economic importance, including a number of high-value timber applications and as the primary species used to cooper barrels for aging distilled spirits (Stringer & Morris, 2022; Dhungel et al., 2023). However, few studies have addressed the genomic diversity of Q. alba, and a lack of available genetic and genomic resources currently presents barriers to furthering the understanding of white oak biology and evolutionary history.

Quercus (Fagaceae) comprises c. 500 species, often divided into two subgenera: Cerris and Quercus (Hipp et al., 2020). The latter is typically further divided into the white oaks (section Quercus), to which Q. alba belongs, and the red oaks (section Lobatae). The phylogeny of oaks has been the focus of several recent studies utilizing reduced representation genome sequencing (Sork et al., 2016; Hipp et al., 2020; Manos & Hipp, 2021), which have clarified some relationships within section Quercus. However, phylogenetic inference in oaks is likely complicated by the suggested prevalence of hybridization and introgression in the group (e.g. McVay et al., 2017; Lazic et al., 2021).

The first published oak genome was that of Quercus robur L. (Plomion et al., 2016a), the pedunculate oak, which is common throughout western Eurasia. To date, there have been at least 11 Quercus species with published chromosome-scale genomes, including four annotated genomes from the white oak clade (Plomion et al., 2016a; Ai et al., 2022; Han et al., 2022; Liu et al., 2022, 2024; Sork et al., 2022; Zhou et al., 2022; Kapoor et al., 2023; L. Wang et al., 2023; W. Wang et al., 2023). This growing number of annotated genomes allows for comparative analyses of gene content and inferences of genome evolution across the oak phylogeny.

Disease resistance-related genes (R genes) have been a focus of genomic studies on oaks and other tree species because of their central role in plant immunity to pathogens (Plomion et al., 2018; Ai et al., 2022; Sork et al., 2022). Resistance genes confer defense against various viral, bacterial, and eukaryotic pathogens by encoding proteins that recognize pathogen-related molecules and trigger downstream immune responses. Plomion et al. (2018) suggested that an expansion of R genes might be at least partly responsible for allowing tree species to live for multiple centuries. Ai et al. (2022) found that the Quercus mongolica Fisch. ex Ledeb. genome assembly contained far fewer putative R genes than the earlier genome assemblies of Quercus lobata Née, Q. robur L., and Quercus suber L. However, the history of how these R gene families have evolved across the oak phylogeny remains poorly understood.

In addition to providing insights into fundamental questions about plant evolution, improving the understanding of genomes across the white oak clade may benefit tree breeding and genetic improvement efforts and help land managers plan for and address global change. Q. alba faces declining seedling recruitment in many parts of its range (Dhungel et al., 2023), which may have implications for ecosystem function throughout eastern North America. Furthermore, anthropogenic climate change is causing a mismatch between populations and their historical climates (Piao et al., 2019; Kijowska-Oberc et al., 2020). The amount of standing genetic variation and the extent to which populations are locally adapted will have implications for the response of Q. alba and other white oak species to global climate change.

Here, we report the first assembled genome of Q. alba and use this new resource to study the evolution of oak genomes. Specifically, we address the following questions. What is the extent of genetic diversity and population differentiation within Q. alba? Are previous phylogenetic hypotheses for the relationships among oak species supported by whole genome data? How have gene content and disease resistance genes evolved during the history of Quercus and related taxa? The answers to these questions will provide a roadmap for future work on the white oak group as a model clade for studying genome evolution and adaptation in highly outcrossing forest trees.