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Evolutionary insights on C4 photosynthetic subtypes in grasses from genomics and phylogenetics.

ABSTRACT: In plants, an oligogene family encodes NADP-malic enzymes (NADP-me), which are responsible for various functions and exhibit different kinetics and expression patterns. In particular, a chloroplast isoform of NADP-me plays a key role in one of the three biochemical subtypes of C(4) photosynthesis, an adaptation to warm environments that evolved several times independently during angiosperm diversification. By combining genomic and phylogenetic approaches, this study aimed at identifying the molecular mechanisms linked to the recurrent evolutions of C(4)-specific NADP-me in grasses (Poaceae). Genes encoding NADP-me (nadpme) were retrieved from genomes of model grasses and isolated from a large sample of C(3) and C(4) grasses. Genomic and phylogenetic analyses showed that 1) the grass nadpme gene family is composed of four main lineages, one of which is expressed in plastids (nadpme-IV), 2) C(4)-specific NADP-me evolved at least five times independently from nadpme-IV, and 3) some codons driven by positive selection underwent parallel changes during the multiple C(4) origins. The C(4) NADP-me being expressed in chloroplasts probably constrained its recurrent evolutions from the only plastid nadpme lineage and this common starting point limited the number of evolutionary paths toward a C(4) optimized enzyme, resulting in genetic convergence. In light of the history of nadpme genes, an evolutionary scenario of the C(4) phenotype using NADP-me is discussed.

SUBMITTER: Christin PA

PROVIDER: S-EPMC2817415 | biostudies-literature | 2009 Jul

REPOSITORIES: biostudies-literature

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Evolutionary insights on C4 photosynthetic subtypes in grasses from genomics and phylogenetics.

Christin Pascal-Antoine PA Samaritani Emanuela E Petitpierre Blaise B Salamin Nicolas N Besnard Guillaume G

Genome biology and evolution 20090720

In plants, an oligogene family encodes NADP-malic enzymes (NADP-me), which are responsible for various functions and exhibit different kinetics and expression patterns. In particular, a chloroplast isoform of NADP-me plays a key role in one of the three biochemical subtypes of C(4) photosynthesis, an adaptation to warm environments that evolved several times independently during angiosperm diversification. By combining genomic and phylogenetic approaches, this study aimed at identifying the mole ...[more]

PMID: 20333192

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Project description:C4 photosynthesis affords higher photosynthetic carbon conversion efficiency than C3 photosynthesis and it therefore represents an attractive target for engineering efforts aiming to improve crop productivity. To this end, blueprints are required that reflect C4 metabolism as closely as possible. Such blueprints have been derived from comparative transcriptome analyses of C3 species with related C4 species belonging to the NAD-malic enzyme (NAD-ME) and NADP-ME subgroups of C4 photosynthesis. However, a comparison between C3 and the phosphoenolpyruvate carboxykinase (PEP-CK) subtype of C4 photosynthesis is still missing. An integrative analysis of all three C4 subtypes has also not been possible to date, since no comparison has been available for closely related C3 and PEP-CK C4 species. To generate the data, the guinea grass Megathyrsus maximus, which represents a PEP-CK species, was analysed in comparison with a closely related C3 sister species, Dichanthelium clandestinum, and with publicly available sets of RNA-Seq data from C4 species belonging to the NAD-ME and NADP-ME subgroups. The data indicate that the core C4 cycle of the PEP-CK grass M. maximus is quite similar to that of NAD-ME species with only a few exceptions, such as the subcellular location of transfer acid production and the degree and pattern of up-regulation of genes encoding C4 enzymes. One additional mitochondrial transporter protein was associated with the core cycle. The broad comparison identified sucrose and starch synthesis, as well as the prevention of leakage of C4 cycle intermediates to other metabolic pathways, as critical components of C4 metabolism. Estimation of intercellular transport fluxes indicated that flux between cells is increased by at least two orders of magnitude in C4 species compared with C3 species. In contrast to NAD-ME and NADP-ME species, the transcription of photosynthetic electron transfer proteins was unchanged in PEP-CK. In summary, the PEP-CK blueprint of M. maximus appears to be simpler than those of NAD-ME and NADP-ME plants.

Project description:Background and aimsThe success of C4 plants lies in their ability to attain greater efficiencies of light, water and nitrogen use under high temperature, providing an advantage in arid, hot environments. However, C4 grasses are not necessarily less sensitive to drought than C3 grasses and are proposed to respond with greater metabolic limitations, while the C3 response is predominantly stomatal. The aims of this study were to compare the drought and recovery responses of co-occurring C3 and C4 NADP-ME grasses from the subfamily Panicoideae and to determine stomatal and metabolic contributions to the observed response.MethodsSix species of locally co-occurring grasses, C3) species Alloteropsis semialata subsp. eckloniana, Panicum aequinerve and Panicum ecklonii, and C4 (NADP-ME) species Heteropogon contortus, Themeda triandra and Tristachya leucothrix, were established in pots then subjected to a controlled drought followed by re-watering. Water potentials, leaf gas exchange and the response of photosynthetic rate to internal CO2 concentrations were determined on selected occasions during the drought and re-watering treatments and compared between species and photosynthetic types.Key resultsLeaves of C4 species of grasses maintained their photosynthetic advantage until water deficits became severe, but lost their water-use advantage even under conditions of mild drought. Declining C4 photosynthesis with water deficit was mainly a consequence of metabolic limitations to CO2 assimilation, whereas, in the C3 species, stomatal limitations had a prevailing role in the drought-induced decrease in photosynthesis. The drought-sensitive metabolism of the C4 plants could explain the observed slower recovery of photosynthesis on re-watering, in comparison with C3 plants which recovered a greater proportion of photosynthesis through increased stomatal conductance.ConclusionsWithin the Panicoid grasses, C4 (NADP-ME) species are metabolically more sensitive to drought than C3 species and recover more slowly from drought.

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Evolutionary insights on C4 photosynthetic subtypes in grasses from genomics and phylogenetics.

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Evolutionary insights on C4 photosynthetic subtypes in grasses from genomics and phylogenetics.

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