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Lineage‐Specific Plastid Degradation in Subtribe Gentianinae

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Lineage‐Specific Plastid Degradation in Subtribe Gentianinae Edinburgh Research Explorer Lineage-specific plastid degradation in subtribe Gentianinae (Gentianaceae) Citation for published version: Fu, PC, Sun, SS, Twyford, AD, Li, BB, Zhou, RQ, Chen, SL, Gao, QB & Favre, A 2021, 'Lineage-specific plastid degradation in subtribe Gentianinae (Gentianaceae)', Ecology and Evolution, pp. 1-14. https://doi.org/10.1002/ece3.7281 Digital Object Identifier (DOI): 10.1002/ece3.7281 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: Ecology and Evolution General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 02. Oct. 2021 Received: 11 July 2020 | Revised: 24 December 2020 | Accepted: 4 January 2021 DOI: 10.1002/ece3.7281 ORIGINAL RESEARCH Lineage- specific plastid degradation in subtribe Gentianinae (Gentianaceae) Peng- Cheng Fu1 | Shan- Shan Sun1 | Alex D. Twyford2,3 | Bei- Bei Li1 | Rui- Qi Zhou1 | Shi- Long Chen4,5 | Qing- Bo Gao4,5 | Adrien Favre6 1School of Life Science, Luoyang Normal University, Luoyang, China Abstract 2Ashworth Laboratories, Institute of The structure and sequence of plastid genomes is highly conserved across most land Evolutionary Biology, The University of plants, except for a minority of lineages that show gene loss and genome degrada- Edinburgh, Edinburgh, UK 3Royal Botanic Garden Edinburgh, tion. Understanding the early stages of plastome degradation may provide crucial Edinburgh, UK insights into the repeatability and predictability of genomic evolutionary trends. We 4 Key Laboratory of Adaptation and investigated these trends in subtribe Gentianinae of the Gentianaceae, which en- Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese compasses ca. 450 species distributed around the world, particularly in alpine and Academy of Sciences, Xining, China subalpine environments. We sequenced, assembled, and annotated the plastomes of 5Qinghai Provincial Key Laboratory of Crop 41 species, representing all six genera in subtribe Gentianinae and all main sections Molecular Breeding, Xining, China 6Senckenberg Research Institute and of the species- rich genus Gentiana L. We reconstructed the phylogeny, estimated Natural History Museum, Frankfurt am divergence times, investigated the phylogenetic distribution of putative gene losses, Main, Germany and related these to substitution rate shifts and species’ habitats. We obtained a Correspondence strongly supported topology consistent with earlier studies, with all six genera in Adrien Favre, Senckenberg Research Institute and Natural History Museum, Gentianinae recovered as monophyletic and all main sections of Gentiana having full Frankfurt am Main, Germany. support. While closely related species have very similar plastomes in terms of size and Email: [email protected] structure, independent gene losses, particularly of the ndh complex, have occurred Funding information in multiple clades across the phylogeny. Gene loss was usually associated with a shift National Natural Science Foundation of China, Grant/Award Number: 31600296 in the boundaries of the small single- copy and inverted repeat regions. Substitution to PCF; China Scholarship Council to PCF; rates were variable between clades, with evidence for both elevated and decelerated German Science Foundation, Grant/Award Number: FA1117/1- 2 to AF rate shifts. Independent lineage- specific loss of ndh genes occurred at a wide range of times, from Eocene to Pliocene. Our study illustrates that diverse degradation pat- terns shape the evolution of the plastid in this species- rich plant group. KEYWORDS divergence dating, molecular evolution, ndh complex, plastome, substitution rate, subtribe Gentianinae 1 | INTRODUCTION et al., 2017; Twyford & Ness, 2017). For example, plastid phylog- enomics has resolved some persistent taxonomic uncertainties in The increasing availability of plastid genomes represents a new op- challenging plant groups (e.g., in Rosaceae; Zhang et al., 2017), and portunity to explore molecular evolution in plants (Tonti- Filippini more generally led to a better understanding of major events in plant This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2021;00:1–14. www.ecolevol.org | 1 2 | FU ET AL. evolution (e.g., the consequences of the Jurassic gap; Li et al., 2019). yet their repeated loss and dispensability under benign nonstressful Furthermore, comparing plastome structure among related clades conditions suggests otherwise (Martín & Sabater, 2010; Ruhlman and linking the structural changes with substitution rates can offer et al., 2015; Wang et al., 2006). Many cases of plastid gene loss can clues to the mechanisms driving their evolution. be explained by transfer of functional copies to the nuclear genome In land plants, plastid genomes are usually composed of two (Kleine et al., 2009; Liu et al., 2020; Martin et al., 1998), and this may inverted repeat (IR) regions that are separated by the large single- also be expected for ndh genes. Loss of ndh genes has usually been copy (LSC) region and the small single- copy (SSC) region (Jansen & observed from sparse taxon sampling, as is the case in the genus Ruhlman, 2012). Comparative analysis among closely related taxa Gentiana L. (Sun et al., 2018). As such, we have a limited understanding can provide insights into the microstructural evolution of plastid ge- of the phylogenetic distribution of gene losses and the selection pres- nomes (Mower & Vickrey, 2018), including IR expansion/reduction sures involved in this loss of ndh genes in this genus and many others. (Choi et al., 2019; Weng et al., 2017), sequence inversion (Mower The family Gentianaceae, and in particularly Gentiana, have long et al., 2019), and gene loss (Graham et al., 2017; Song et al., 2017; attracted the attention of scientists because of their medical, chemi- Yao et al., 2019). Plastome microstructural change can also pro- cal, and horticultural value (Ho & Liu, 2001; Rybczyński et al., 2015). vide synapomorphies to support sequence- based phylogenetic Gentiana species are predominantly alpine and occur in numerous results, as seen with the loss of the rpl2 intron in Asteropeiaceae mountain systems around the world (Ho & Liu, 2001). Biogeographic and Physenaceae (Yao et al., 2019). Furthermore, some trends in the studies have shown that the Qinghai– Tibet Plateau (QTP) acted as evolution of plastome structure are known to be associated with the primary source area for Gentiana to disperse to many other dis- changes in nucleotide substitution rates (Weng et al., 2017) and se- tant mountainous areas, and is the center of biodiversity for these lection pressures (Wicke et al., 2016). Elevated substitution rates are species (Favre et al., 2016). Although our understanding of the tax- often associated with changes in plastome size (Schwarz et al., 2017) onomy and phylogenetic relationships within Gentiana and subtribe or in life- history (Gaut et al., 2011). Some remarkable modifications Gentianinae has greatly improved in the past two decades, little is of plastid genomes have been observed in nonphotosynthetic par- known about patterns, trends, and modes of molecular evolution asites (e.g., holoparasitic members of the Orobanchaceae). In these among Gentianinae genera and sections within Gentiana. For exam- species, the functional loss of photosynthetic genes correlates with ple, plastome sequences of species from section Kudoa (Masamune) microstructural changes and accelerated substitution rates due to Satake & Toyokuni ex Toyokuni have revealed contrasting patterns of relaxed selection, resulting in miniaturized plastid genomes with a plastome sequence evolution, with some but not all species showing greatly reduced gene content (Wicke et al., 2016). This plastid ge- notable plastome size decreases and ndh gene losses (Fu et al., 2016; nome degradation starts with small scale losses of nonessential Sun et al., 2018). In contrast, only subtle sequence divergence and genes and the accumulation of microstructural changes, followed by microstructural change are present among species in three other sec- further phases of elevated evolution and gene losses on a trajectory tions (Ni et al., 2017; Sun Wang & Fu, 2019; Sun, Zhou, et al., 2019; of reductive plastome evolution. Zhou et al., 2018). Based on these results, Gentiana and its closely The study of ndh (NADH dehydrogenase- like) genes has provided related genera appear to be a promising system for investigating many useful insights into gene loss, gene degradation, and gene re- plastome evolution and its link to evolutionary transitions, such as tention in plants. The ndh genes produce the NADH complex,
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