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.
Highlights
Chloroplasts evolved from prokaryotic photosynthetic endosymbionts [1] as cell organelles that maintain their own genetic material in a double stranded DNA molecule ranging in size from 35 to 217 kb [2]
The plastome of Najas flexilis codes for 103 unique genes, sixteen of which are duplicated in the inverted repeat regions (Table 1 and Fig. 1)
The rps12 gene is transpliced with exon 1 coded in the large single copy region (LSC) region and exons 2 and 3 in the inverted repeats (IR)
Summary
Chloroplasts evolved from prokaryotic photosynthetic endosymbionts [1] as cell organelles that maintain their own genetic material in a double stranded DNA molecule ranging in size from 35 to 217 kb [2]. Lost in other algal divisions, the ndh genes probably were essential in the adaptation of green algae to the fluctuating conditions of shoreline environments [5] The eleven plastid ndh genes together with four nuclear genes (nhdL, ndhM, ndhN, and ndhO) encode the thylakoid NAD(P)H dehydrogenase complex which functions mainly in the electron transfer from NADH to plastoquinone, which protects the cell against photooxidative-related stress and maintains optimal rates of cyclic photophosphorylation [5]. Recolonization of aquatic environments by land plants has occurred up to 100 independent times, comprising up to 2% of the approximate 350,000 angiosperm species [22] These recolonization events presumably would have required many physiological, metabolic and reproductive adaptations essential to accommodate the broad and novel conditions of aquatic habitats, which range from warm and sunny shallow waters to cool and dark deep waters. Modifications in the chloroplast of Najas flexilis reported here may provide insight on the importance of the plastid NAD(P)H dehydrogenase during land colonization by photosynthetic eukaryotes
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