Strategies of tolerance reflected in two North American maple genomes

Abstract

The first chromosome‐scale assemblies for North American members of the Acer genus, sugar maple (Acer saccharum) and boxelder (Acer negundo), as well as transcriptomic evaluation of the abiotic stress response in A. saccharum are reported. This integrated study describes in‐depth aspects contributing to each species' approach to tolerance and applies current knowledge in many areas of plant genome biology with Acer physiology to help convey the genomic complexities underlying tolerance in broadleaf tree species.

Keywords: Acer negundo; Acer saccharum; abiotic stress; aluminum; calcium; differential expression; genome; nutrient stress; plasticity; tolerance.

Figure 1

(a) Native distributions of Acer saccharum (blue) and Acer negundo (orange) in North America. Leaves indicate locations of individuals selected for the reference genomes: A. saccharum from the University of Maryland campus and A. negundo from the Smithsonian Environmental Research Center. Hubbard Brook Experimental Forest (HBEF) is the location of the nine individuals used for RNA‐Seq. (b) All records of occurrence, native, introduced, and unknown, per BIEN 4.2. Non‐native occurrences are predominantly A. negundo. [Colour figure can be viewed at wileyonlinelibrary.com]

Figure 2

Results of assembly testing with Acer saccharum, comparing fragmentation in terms of total contigs versus assembly length. The dashed line represents the estimated genome size. Gray dots are short‐read assemblers, shown as highly fragmented. Blue dots are long‐read tests of assembly workflows. Canu refers to the use of reads error‐corrected by the Canu pipeline. The red dot is the selected draft assembly, and the green dot shows scaffolding results following Hi‐C. Detailed assembly statistics are available in Data S1. [Colour figure can be viewed at wileyonlinelibrary.com]

Figure 3

Ks distribution for WGD synteny blocks with a summary of duplication types in (a) Acer negundo and (b) Acer saccharum. Abbreviations for categories of duplication: WGD, whole genome duplication; TD, tandem duplication; PD, proximal duplication; TRD, transposed duplication; DSD, dispersed duplication. (c) Circos plot of the 13 chromosomes ordered largest to smallest for A. negundo (orange bars) and A. saccharum (blue bars) with distributions of gene density (green) and transposable element frequency (purple). Syntenic regions are linked in gray with darker shades to visually highlight larger recombinations. [Colour figure can be viewed at wileyonlinelibrary.com]

Figure 4

(a) Differential expression study design showing the number of samples collected in fall and spring from treatment plots at the Hubbard Brook Experimental Forest, Nutrient Perturbation study. (b) Differentially expressed genes (up‐ and downregulated) for each treatment and season comparison. Charts display both significance and relative expression denoted as log‐fold change. Dotted lines indicate thresholds of significance (0.1 P‐adjusted, 1.5 log₂ fold change). [Colour figure can be viewed at wileyonlinelibrary.com]

Figure 5

(a) Gene ontology enrichments for Acer (all three species combined), Acer negundo, and Acer saccharum. Abbreviations for gene family dynamics: E, expanded; N, novel; RC, rapidly contracting. (b) Total gene families, shared and unique, among the Acer. (c) Reconstructed gene tree showing contracted gene families in red and expanded in green. [Colour figure can be viewed at wileyonlinelibrary.com]

Figure 6

Orthogroup sizes for aluminum tolerance gene families are presented by species. Families were selected for inclusion based on documented aluminum tolerance and/or presence in the HBEF RNA‐Seq differential expression results. Color represents the proportion of gene membership per species, with darker purple equating to more contracted families relative to the median and dark green indicating expansion. H, family contains HBEF differentially expressed gene; E, expanded in Acer saccharum; C, contracting; M, missing; N, novel; *, rapidly expanding. Categorization of tolerance is according to literature describing aluminum stress phenotypes. The undetermined category contains species where tolerance to aluminum or acidic soils has not been reported. ¹ Betula pendula is undetermined due to high variability in tolerance by genotype. [Colour figure can be viewed at wileyonlinelibrary.com]

Figure 7

Acer negundo gene families with ontology related to DNA damage and repair, and secondary enrichments categorized by color. Circles with multiple colors indicate multiple ontology assignments. Lines indicate known or predicted interactions or other associations as determined based on text mining, co‐expression, or protein homology. [Colour figure can be viewed at wileyonlinelibrary.com]