Plastid Genomes of Five Species of Riverweeds (Podostemaceae): Structural Organization and Comparative Analysis in Malpighiales

Abstract

With the advent of next-generation sequencing technologies, whole-plastome data can be obtained as a byproduct of low-coverage sequencing of the plant genomic DNA. This provides an opportunity to study plastid evolution across groups, as well as testing phylogenetic relationships among taxa. Within the order Malpighiales (∼16,000 spp.), the Podostemaceae (∼300 spp.) stand out for their unique habit, living attached to rocks in fast-flowing aquatic habitats, and displaying highly modified morphologies that confound our understanding of their classification, biology, and evolution. In this study, we used genome skimming data to assemble the full plastid genome of 5 species within Podostemaceae. We analyzed our data in a comparative framework within Malpighiales to determine the structure, gene content, and rearrangements in the plastomes of the family. The Podostemaceae have one of the smallest plastid genomes reported so far for the Malpighiales, possibly due to variation in length of inverted repeat (IR) regions, gene loss, and intergenic region variation. We also detected a major inversion in the large single-copy region unique to the family. The uncommon loss or pseudogenization of ycf1 and ycf2 in angiosperms and in land plants in general is also found to be characteristic of Podostemaceae, but the compensatory mechanisms and implications of this and of the pseudogenization of accD , rpl22 , and clpP and loss of rps16 remain to be explained in this group. In addition, we estimated a phylogenetic tree among selected species in Malpighiales. Our findings indicate that the Podostemaceae are a distinct lineage with long branches that suggest faster rates of evolution in the plastome of the group, compared with other taxa in the order. This study lays the foundations for future phylogenomic studies in the family.

Insights into chloroplast genome variation across Opuntioideae (Cactaceae)

“…All genes here reported as pseudogenes in the O. quimilo plastome (accD, rpl16, rps16, ycf1 and ycf2) have also been reported as pseudogenes in the Mammillaria plastomes (Solórzano et al 2019), while the accD was described as a pseudogene in Carnegia gigantea (Sanderson et al 2015). Pseudogenization of these genes has been repeatedly reported across different angiosperm lineages, such as Malpighiales, Campanulales, Ericales, Poales, Solanales, Geraniales, Santalales and Myrtales (Harris et al 2013;Haberle et al 2008;Fajardo et al 2013;Weng et al 2013;Bedoya et al 2019;Cui et al 2019;Machado et al 2017). Even though these genes have been identified with essential functions beyond photosynthesis and retained in the plastome of most embryophytes (Drescher et al, 2000;Kuroda and Maliga, 2003;Kode et al, 2005;Kikuchi et al, 2013;Parker et al, 2014;Dong et al, 2015), there are several other plants where these genes are missing from the chloroplast genome (Kim, 2004;Magee et al, 2010;Lei et al, 2016;Graham et al, 2017).…”

Degradation of key photosynthetic genes in the critically endangered semi-aquatic flowering plant Saniculiphyllum guangxiense (Saxifragaceae)

“…Although chloroplast genome evolution in Saxifragales has been previously understood as very conservative [26], further sampling has revealed surprising plastid variation in one of its rarest and most unusual lineages. Similar but less extreme patterns of gene loss have been observed before in aquatic members of order Alismatales and Podostemaceae, and appear to represent multiple independent evolutionary events [1, 3], suggesting a possible relationship with life history. Nevertheless, this putative correlation is imperfect; unlike the partly aerial Saniculiphyllum , Alismatales contains some of the most thoroughly aquatic-adapted angiosperms, including the only examples of aquatic pollination [1].…”

“…Most losses of plastid gene function have been associated with parasitic and mycoheterotrophic plants, which presumably have few functional constraints on photosynthetic gene evolution. Degradation of genes in the NDH complex has nevertheless been observed in several fully photosynthetic lineages with a variety of life history traits: woody perennials in Pinaceae and Gnetales (both gymnosperms), short-lived perennials in Geraniaceae (eudicots: rosids), carnivorous and often aquatic plants of Lentibulariaceae (eudicots: asterids), various photosynthetic members of Orchidaceae (monocot), and aquatic members of Alismatales (monocot) and Podostemataceae (rosid; [1, 3, 6, 7, 14–17]). The primary function of the NDH complex is thought to be reduction of photooxidative stress under fluctuating light conditions.…”

“…Accumulating evidence, however, has increasingly documented the loss of “accessory” photosynthetic genes, only conditionally essential under stress, in fully photosynthetic plants. Although not universal, many of these losses are associated with highly specialized life history traits such as aquatic habit [1–3], carnivory [4, 5], and a mycoheterotrophic life-stage [6]; the functional significance of these losses remains enigmatic [7].…”

A Repertory of Rearrangements and the Loss of an Inverted Repeat Region in Passiflora Chloroplast Genomes

“…These rearrangements are well documented, for instance, in Hevea brasiliensis (Euphorbiaceae) ( Tangphatsornruang et al. 2011 ) and in species of riverweeds (Podostemaceae) ( Bedoya et al. 2019 ), both families belonging to the Malpighiales.…”