Independent recruitment of duplicated β-subunit-coding NAD-ME genes aided the evolution of C4 photosynthesis in Cleomaceae
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In different lineages of C4 plants, the release of CO2 by decarboxylation of a C4 acid
near rubisco is catalyzed by NADP-malic enzyme (ME) or NAD-ME, and the facultative
use of phosphoenolpyruvate carboxykinase. The co-option of gene lineages during the
evolution of C4-NADP-ME has been thoroughly investigated, whereas that of C4-NAD ME has received less attention. In this work, we aimed at elucidating the mechanism of
recruitment of NAD-ME for its function in the C4 pathway by focusing on the eudicot
family Cleomaceae. We identified a duplication of NAD-ME in vascular plants that
generated the two paralogs lineages: α- and β-NAD-ME. Both gene lineages were
retained across seed plants, and their fixation was likely driven by a degenerative
process of sub-functionalization, which resulted in a NAD-ME operating primarily as
a heteromer of α- and β-subunits. We found most angiosperm genomes maintain a 1:1
β-NAD-ME/α-NAD-ME (β/α) relative gene dosage, but with some notable exceptions
mainly due to additional duplications of β-NAD-ME subunits. For example, a significantly
high proportion of species with C4-NAD-ME-type photosynthesis have a non-1:1 ratio
of β/α. In the Brassicales, we found C4 species with a 2:1 ratio due to a β-NAD-ME
duplication (β1 and β2); this was also observed in the C3 Tarenaya hassleriana and
Brassica crops. In the independently evolved C4 species, Gynandropsis gynandra and
Cleome angustifolia, all three genes were affected by C4 evolution with α- and β1-
NAD-ME driven by adaptive selection. In particular, the β1-NAD-MEs possess many
differentially substituted amino acids compared with other species and the β2-NAD-MEs
of the same species. Five of these amino acids are identically substituted in β1-NAD-ME
of G. gynandra and C. angustifolia, two of them were identified as positively selected.
Using synteny analysis, we established that β-NAD-ME duplications were derived from
ancient polyploidy events and that α-NAD-ME is in a unique syntenic context in both
Cleomaceae and Brassicaceae. We discuss our hypotheses for the evolution of NAD-ME and its recruitment for C4 photosynthesis. We propose that gene duplications provided the basis for the recruitment of NAD-ME in C4 Cleomaceae and that all
members of the NAD-ME gene family have been adapted to fit the C4-biochemistry.
Also, one of the β-NAD-ME gene copies was independently co-opted for its function in
the C4 pathway.
Para citar este articulo: Tronconi MA, Hüdig M, Schranz ME and Maurino VG (2020) Independent Recruitment of Duplicated β-Subunit-Coding NAD-ME Genes Aided the Evolution of C4 Photosynthesis in Cleomaceae. Front. Plant Sci. 11:572080. doi: 10.3389/fpls.2020.572080
Para citar este articulo: Tronconi MA, Hüdig M, Schranz ME and Maurino VG (2020) Independent Recruitment of Duplicated β-Subunit-Coding NAD-ME Genes Aided the Evolution of C4 Photosynthesis in Cleomaceae. Front. Plant Sci. 11:572080. doi: 10.3389/fpls.2020.572080
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