Mutational Dynamics of Aroid Chloroplast Genomes II

Mutational Dynamics of Aroid Chloroplast Genomes II

fgene-11-610838 January 13, 2021 Time: 17:16 # 1 BRIEF RESEARCH REPORT published: 20 January 2021 doi: 10.3389/fgene.2020.610838 Mutational Dynamics of Aroid Chloroplast Genomes II Abdullah1†, Claudia L. Henriquez2, Thomas B. Croat3, Peter Poczai4*‡ and Ibrar Ahmed5*‡ 1 Department of Biochemistry, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad, Pakistan, 2 Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, CA, United States, 3 Missouri Botanical Garden, St. Louis, MO, United States, 4 Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland, 5 Alpha Genomics Private Limited, Islamabad, Pakistan The co-occurrence among single nucleotide polymorphisms (SNPs), insertions- deletions (InDels), and oligonucleotide repeats has been reported in prokaryote, eukaryote, and chloroplast genomes. Correlations among SNPs, InDels, and repeats Edited by: have been investigated in the plant family Araceae previously using pair-wise sequence Madhav P. Nepal, alignments of the chloroplast genomes of two morphotypes of one species, Colocasia South Dakota State University, United States esculenta belonging to subfamily Aroideae (crown group), and four species from the Reviewed by: subfamily Lemnoideae, a basal group. The family Araceae is a large family comprising Sarbottam Piya, 3,645 species in 144 genera, grouped into eight subfamilies. In the current study, we The University of Tennessee, performed 34 comparisons using 27 species from 7 subfamilies of Araceae to determine Knoxville, United States Ueric José Borges de Souza, correlation coefficients among the mutational events at the family, subfamily, and genus Federal University of Tocantins, Brazil levels. We express strength of the correlations as: negligible or very weak (0.10–0.19), *Correspondence: weak (0.20–0.29), moderate (0.30–0.39), strong (0.40–0.69), very strong (0.70–0.99), Peter Poczai peter.poczai@helsinki.fi and perfect (1.00). We observed strong/very strong correlations in most comparisons, Ibrar Ahmed whereas a few comparisons showed moderate correlations. The average correlation [email protected] coefficient was recorded as 0.66 between “SNPs and InDels,” 0.50 between “InDels † ORCID: and repeats,” and 0.42 between “SNPs and repeats.” In qualitative analyses, 95–100% Abdullah orcid.org/0000-0003-1628-8478 of the repeats at family and sub-family level, while 36–86% of the repeats at genus ‡These authors have contributed level comparisons co-occurred with SNPs in the same bins. Our findings show that equally to this work such correlations among mutational events exist throughout Araceae and support the Specialty section: hypothesis of distribution of oligonucleotide repeats as a proxy for mutational hotspots. This article was submitted to Keywords: Araceae (aroid), chloroplast genome, correlations, repeats, InDels (insertions/deletions) Plant Genomics, a section of the journal Frontiers in Genetics INTRODUCTION Received: 27 September 2020 Accepted: 16 November 2020 The chloroplast (cp) is a double-membrane bound organelle in plants, which plays an important Published: 20 January 2021 role in photosynthesis (Daniell et al., 2016). The chloroplast genome originated from prokaryotes Citation: (Palmer, 1985). It shows uniparental inheritance, maternal in most angiosperms and paternal in Abdullah, Henriquez CL, some gymnosperms (Neale and Sederoff, 1989; Avni and Edelman, 1991). Many mutational events Croat TB, Poczai P and Ahmed I (2021) Mutational Dynamics of Aroid occur in the cp genome, including InDels, SNPs, inversions, tandem repeats, and oligonucleotide Chloroplast Genomes II. repeats (Poczai and Hyvönen, 2011; Jheng et al., 2012; Xu et al., 2015; Abdullah et al., 2019; Front. Genet. 11:610838. Iram et al., 2019; Sablok et al., 2019). Sufficient polymorphism and uniparental inheritance doi: 10.3389/fgene.2020.610838 make the chloroplast genome suitable for phylogenetic inference, resolution of taxonomic Frontiers in Genetics| www.frontiersin.org 1 January 2021| Volume 11| Article 610838 fgene-11-610838 January 13, 2021 Time: 17:16 # 2 Abdullah et al. Mutational Dynamics of Aroid discrepancies, population genetics, barcoding, and estimation Lemnoideae produce bisexual flowers and inhabit aquatic habitat of time of lineage divergence (Poczai et al., 2011; Ahmed, (Mayo et al., 1997; Cusimano et al., 2011). These species also 2014; Poczai and Hyvönen, 2017; Mehmood et al., 2020c; demonstrated a different rate of mutations, which is consistent Shahzadi et al., 2020). with the finding that aquatic and tropical plant have diverse Previously, co-existence of mutations was observed among mutation rates (Abbasi et al., 2016; Hu et al., 2017; Hart et al., SNPs, InDels, and repeats in prokaryotic and eukaryotic genomes 2019; Wang et al., 2020). Sampling is therefore sparse in the (Silva and Kondrashov, 2002; Hardison et al., 2003; Tian et al., previous study for a large and ancient monocot family like 2008; Chen et al., 2009; Zhu et al., 2009; McDonald et al., 2011). Araceae, which dates back to the Early Cretaceous period, Three alternate hypotheses were suggested to explain the co- and is divided into eight diverse subfamilies distributed across existence of mutations. First, the “regional difference hypothesis” the multitude of ecological habitats (Cusimano et al., 2011; suggests that certain regions are more prone to mutations Nauheimer et al., 2012; Henriquez et al., 2014). This family in comparison to other regions (Silva and Kondrashov, 2002; comprises 144 genera and 3,645 species (Boyce and Croat, 2018). Hardison et al., 2003). The second, “InDel-induced mutation Recently, with the advancement of next generation sequencing, hypothesis” was suggested based on strong association between chloroplast genome sequences of several species of Araceae were InDels and substitutions, which suggested the recruitment of reported from subfamilies Aroideae, Lasioideae, Pothoideae, error-prone DNA polymerase at point of InDels is the cause of Monsteroideae, Orontioideae, and Zamioculcadoideae (Han generation of substitutions (Tian et al., 2008; Yang et al., 2009). et al., 2016; Choi et al., 2017; Kim et al., 2019; Abdullah et al., The third hypothesis suggests high frequency of oligonucleotide 2020a,b; Henriquez et al., 2020a,b). We included 27 species repeats in a region of the genome generates InDels and from 7 subfamilies of Araceae which are diverse in term of substitutions (McDonald et al., 2011). To repair DNA damage, habit, habitat, native range, and evolutionary time of divergence the existence of a high number of repeats in a region leads (Table 1 and Figure 1A). The availability of these genomic to the recruitment of error-prone DNA polymerases, thus the resources from a wide array of aroid species (Table 1) provided adjacent sequences replicate with a higher error rate compared enough data to elucidate correlations among substitutions, to other regions (McDonald et al., 2011). Hence, instead of InDels, and repeats throughout the family. InDel per se, this hypothesis places more importance on “regional In the current study, we are interested in determining difference hypothesis.” correlations among these mutational events throughout the Associations have been reported between SNPs, repeats, family Araceae using genus-, subfamily-, and family-level InDels, and inversions (Mes et al., 2000; Lockhart et al., 2001; comparisons, aka time of divergences ranged from relatively Li J. et al., 2018). The role of repeats in the generation of recent splits to deep divergences. This study will be helpful to inversions (Kim and Lee, 2005; Whitlock et al., 2010) and InDels understand whether such correlations exist among these five (Kawata et al., 1997) has also been reported. However, these species used in Ahmed et al.(2012) by chance or whether these observations were made on the bases of few loci instead of correlations exist among species of Araceae at varying taxonomic complete chloroplast genomes. The first study of associations levels and diverse ecological habitats. among SNPs, InDels, and repeats based on genome-wide analyses of complete chloroplast genomes included five species of Araceae (Ahmed et al., 2012). That study suggests the distribution of MATERIALS AND METHODS oligonucleotide repeats could be used as a proxy for mutational hotspots. Following Ahmed et al.(2012), correlations were We downloaded chloroplast genome sequences of 27 species of studied in two species of genus Cephalotaxus Siebold & Zucc. Araceae from GenBank of the National Center for Biotechnology ex Endl. (Yi et al., 2013). However, authors observed very Information (Table 1). The species are high diverse in terms weak correlations between “InDels and SNPs” and “repeats and of habitat, geographical distribution, ecology, and evolutionary InDels,” whereas moderate correlation was observed between history. The species included in the comparisons range in “substitutions and repeats.” Recently, strong correlations were distribution from tropical and subtropical to temperate regions reported among these mutational events in the species of genus of the world, such as America, Asia, and Africa (Table 1). Dendrobium Sw. (Li et al., 2020), whereas others have described Similarly, these species also differed in terms of habit and weak to strong correlations in species of the plant family habitat occupying aquatic and semi-aquatic to tropical and Malvaceae (Abdullah et al., 2020c,d). Hence, the very thorough subtropical forests (Table 1).

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