The Plastid Genome of Najas flexilis: Adaptation to Submersed Environments Is Accompanied by the Complete Loss of the NDH Complex in an Aquatic Angiosperm

Abstract

The re-colonization of aquatic habitats by angiosperms has presented a difficult challenge to plants whose long evolutionary history primarily reflects adaptations to terrestrial conditions. Many aquatics must complete vital stages of their life cycle on the water surface by means of floating or emergent leaves and flowers. Only a few species, mainly within the order Alismatales, are able to complete all aspects of their life cycle including pollination, entirely underwater. Water-pollinated Alismatales include seagrasses and water nymphs (Najas), the latter being the only freshwater genus in the family Hydrocharitaceae with subsurface water-pollination. We have determined the complete nucleotide sequence of the plastid genome of Najas flexilis. The plastid genome of N. flexilis is a circular AT-rich DNA molecule of 156 kb, which displays a quadripartite structure with two inverted repeats (IR) separating the large single copy (LSC) from the small single copy (SSC) regions. In N. flexilis, as in other Alismatales, the rps19 and trnH genes are localized in the LSC region instead of within the IR regions as in other monocots. However, the N. flexilis plastid genome presents some anomalous modifications. The size of the SSC region is only one third of that reported for closely related species. The number of genes in the plastid is considerably less. Both features are due to loss of the eleven ndh genes in the Najas flexilis plastid. In angiosperms, the absence of ndh genes has been related mainly to the loss of photosynthetic function in parasitic plants. The ndh genes encode the NAD(P)H dehydrogenase complex, believed essential in terrestrial environments, where it increases photosynthetic efficiency in variable light intensities. The modified structure of the N. flexilis plastid genome suggests that adaptation to submersed environments, where light is scarce, has involved the loss of the NDH complex in at least some photosynthetic angiosperms.

High Connectivity Among Synedrella nodiflora Populations in Java Island Based on Intergenic Spacer atpB-rbcL

“…Nevertheless, the circular chloroplast genomes of most seed plant species are highly conserved in terms of gene arrangement. In general, they consist of a large single copy (LSC) and a small single copy (SSC) regions, which are separated from each other by two long identical but in an opposite direction sequences known as the inverted repeats (IR) (Peredo et al, 2013;Wang et al, 2013). The size of chloroplast genome ranges from 120 to 220 kb, where variation in size is caused usually by the enlargement or reduction of the IR influencing LSC or SSC nearby.…”

Plastid phylogenomics and molecular evolution of Alismatales

“…() and Peredo et al. () hypothesized that loss of plastid NADH dehydrogenase function is tenable in submerged habitats, if there is reduced photooxidative stresses in subtidal zones. However, the far slower rates of carbon dioxide diffusion in water versus air may actually increase the likelihood of photooxidative stress in submerged aquatics, by starving them of carbon dioxide, unless such plants are also well‐shaded.…”

“…Les et al, 1997), functional loss of the enzyme complex must not be a prerequisite for survival in a submersed marine environment. A third loss was hypothesized by Iles et al (2013) to have occurred in the common ancestor of Najas, Thalassia and Vallisneria in Hydrocharitaceae (see also Peredo et al, 2013; who confirmed the loss in Najas). Our expanded taxon and gene sampling clarifies the taxonomic extent of the loss in Hydrocharitaceae (Fig.…”

“…In Alismatales, a comprehensive set of plastid genome data would be particularly well suited for investigating the molecular evolution of plastid NADH dehydrogenase, a major plastid protein complex coded for primarily by multiple genes in the plastid genome, which appears to function in regulating cyclical electron transport and in dealing with photooxidative stress (Martin and Sabater, ; and see below). Multiple genes for subunits in this complex have been lost or pseudogenized several times in the order, consistent with repeated loss of enzyme function (Iles et al., ; Peredo et al., ).…”

The Complete Plastid Genome Sequence of Iris gatesii (Section Oncocyclus), a Bearded Species from Southeastern Turkey

“…Iris is a diverse genus with bearded and non-bearded species; species with rhizomes, bulbs, or tuberous roots; mesic and xeric species; and species with unifacial or dorsiventral leaves that may be large and obvious or reduced and only a few centimeters tall. Researchers have found divergent plastid genomes that may be related to habitat or plant life form (Delannoy et al 2011;Logacheva et al 2011;Wang and Messing 2011;Peredo et al 2013). The diversity of habitats utilized and morphological forms present in Iris provides an opportunity to explore plastid genome diversity between sister clades and among more distantly related clades across diverse plant forms and modes of habitat utilization.…”