Genomic Convergence in the Adaptation to Extreme Environments

Abstract

Convergent evolution is especially common in plants that have independently adapted to the same extreme environments (i.e., extremophile plants). The recent burst of omics data has alleviated many limitations that have hampered molecular convergence studies of non-model extremophile plants. In this review, we summarize cases of genomic convergence in these taxa to examine the extent and type of genomic convergence during the process of adaptation to extreme environments. Despite being well studied by candidate gene approaches, convergent evolution at individual sites is rare and often has a high false-positive rate when assessed in whole genomes. By contrast, genomic convergence at higher genetic levels has been detected during adaptation to the same extreme environments. Examples include the convergence of biological pathways and changes in gene expression, gene copy number, amino acid usage, and GC content. Higher convergence levels play important roles in the adaptive evolution of extremophiles and may be more frequent and involve more genes. In several cases, multiple types of convergence events have been found to co-occur. However, empirical and theoretical studies of this higher level convergent evolution are still limited. In conclusion, both the development of powerful approaches and the detection of convergence at various genetic levels are needed to further reveal the genetic mechanisms of plant adaptation to extreme environments.

Keywords: adaptive evolution; convergent evolution; extreme environments; plant genomes.

Figure 1

Types of Genomic Convergence. We classify genomic convergence as events that affect nucleotide substitutions at individual sites, gene copy number, gene expression alteration, and genome composition. The source data, detection methods, and examples are shown for each type. See Box 1 for details of detection methods. The examples in (A) and (C) are adapted from Yang et al. (2017). The examples in (B) and (D) are based on data from Ma et al. (2013), Wu et al. (2012), Yang et al. (2013) and Lyu et al. (2018).

Figure 2

Multi-level Convergence of Mangrove Genomes. (A) Examples of convergent AA substitutions in three mangrove genomes. Each of the three genes contains at least three convergent AA substitutions and participates in salinity tolerance. (B) Convergence of AA usage in mangrove genomes. The AA usage of the three mangrove genomes is distinct from that of more than 50 inland dicotyledon genomes. The five most underused AAs are shown on the left (blue font) and the four most overused in mangroves are shown on the right (red font). (C) The numbers of long terminal repeat-retrotransposons (LTR-RTs) in the three mangrove genomes are convergently smaller than those of their inland relatives. (A) and (B) are based on data from He et al., 2020a; (C) is based on data from Lyu et al. (2018).