J Syst Evol ›› 2023, Vol. 61 ›› Issue (2): 328-344.DOI: 10.1111/jse.12854

• Research Articles • Previous Articles     Next Articles

Mutational meltdown or controlled chain reaction: The dynamics of rapid plastome evolution in the hyperdiversity of Poaceae

Jie Wang1,2†, Gao‐Fei Fu1,2†, Luke R. Tembrock3†, Xue‐Zhu Liao1, Song Ge4, and Zhi‐Qiang Wu1,2*   

  1. 1 Kunpeng Institute of Modern Agriculture at Foshan, Foshan 528200, Guangdong, China
    2 Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Shenzhen 518120, Guangdong, China
    3 Department of Agricultural Biology, Colorado State University, Fort Collins, CO 80523, USA
    4 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
    These authors contributed equally to this study.
    *Author for correspondence. E‐mail: wuzhiqiang@caas.cn
  • Received:2022-02-19 Accepted:2022-04-11 Online:2022-04-18 Published:2023-03-01

Abstract: The study of genomic structural evolution associated with accelerated evolutionary rates that result in avoidance of meltdown and increase biodiversity is becoming ever more possible as the number of available plastomes increases. To more comprehensively analyze rate heterogeneity among monocots and within Poaceae, we sequenced plastomes from four Poaceae species, combined them with publicly available data from ~200 plastomes, and conducted comparative analyses to quantify the pattern of rate heterogeneity between different lineages, functional groups, and periods of evolutionary time. We compared structural differences across the Poaceae to quantify how changes in plastome size correspond to different genomic subunits and the evolution of IR–SC junction boundaries. The substitution rates among ancestral Poaceae were inferred to be exceptionally rapid compared to other monocots but slowed after divergence into extant lineages, which could not be sufficiently explained by positive selection. As such, rapid rates in the ancestral lineage leading to Poaceae might be more closely linked to large-scale structural changes like the loss of ycf1 and ycf2. The total increase in plastome size across Poaceae was positively correlated with the total length of intergenic spacers, tandem repeats, and dispersed repeats as well as large single copy, and inverted repeats (IRs). The continuous evolution of IR–SC junction boundaries was asynchronous with sizes of total genome and subunits across Poaceae. Future work is needed to better understand what factors in ancestral Poaceae evolved to harness such rapid rates of plastome evolution, avoid a mutational meltdown, and escape the stagnation of strong purifying selection as well as if these factors could be utilized to synthetically control rates.

Key words: C4 photosynthesis, evolutionary rate, inverted repeats, monocots, plastome size