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Plant Physiol. 2017 Mar;173(3):1648-1658. doi: 10.1104/pp.16.01893. Epub 2017 Feb 2.

Loss of the Chloroplast Transit Peptide from an Ancestral C3 Carbonic Anhydrase Is Associated with C4 Evolution in the Grass Genus Neurachne.

Clayton H1,2,3, Saladié M1,2,3, Rolland V1,2,3, Sharwood R1,2,3, Macfarlane T1,2,3, Ludwig M4,5,6.

Author information

1
School of Molecular Sciences, University of Western Australia, Perth, Western Australia 6009, Australia (H.C., M.S., M.L.).
2
Australian Research Council Centre for Translational Photosynthesis, Research School of Biology, Australian National University, Canberra, Australian Capital Territory 2601, Australia (V.R., R.S.); and.
3
Western Australian Herbarium, Science and Conservation Division, Department of Parks and Wildlife, Perth, Western Australia 6152, Australia (T.M.).
4
School of Molecular Sciences, University of Western Australia, Perth, Western Australia 6009, Australia (H.C., M.S., M.L.); martha.ludwig@uwa.edu.au.
5
Australian Research Council Centre for Translational Photosynthesis, Research School of Biology, Australian National University, Canberra, Australian Capital Territory 2601, Australia (V.R., R.S.); and martha.ludwig@uwa.edu.au.
6
Western Australian Herbarium, Science and Conservation Division, Department of Parks and Wildlife, Perth, Western Australia 6152, Australia (T.M.) martha.ludwig@uwa.edu.au.

Abstract

Neurachne is the only known grass lineage containing closely related C3, C3-C4 intermediate, and C4 species, making it an ideal taxon with which to study the evolution of C4 photosynthesis in the grasses. To begin dissecting the molecular changes that led to the evolution of C4 photosynthesis in this group, the complementary DNAs encoding four distinct β-carbonic anhydrase (CA) isoforms were characterized from leaf tissue of Neurachne munroi (C4), Neurachne minor (C3-C4), and Neurachne alopecuroidea (C3). Two genes (CA1 and CA2) each encode two different isoforms: CA1a/CA1b and CA2a/CA2b. Transcript analyses found that CA1 messenger RNAs were significantly more abundant than transcripts from the CA2 gene in the leaves of each species examined, constituting ∼99% of all β-CA transcripts measured. Localization experiments using green fluorescent protein fusion constructs showed that, while CA1b is a cytosolic CA in all three species, the CA1a proteins are differentially localized. The N. alopecuroidea and N. minor CA1a isoforms were imported into chloroplasts of Nicotiana benthamiana leaf cells, whereas N. munroi CA1a localized to the cytosol. Sequence analysis indicated an 11-amino acid deletion in the amino terminus of N. munroi CA1a relative to the C3 and C3-C4 proteins, suggesting that chloroplast targeting of CA1a is the ancestral state and that loss of a functional chloroplast transit peptide in N. munroi CA1a is associated with the evolution of C4 photosynthesis in Neurachne spp. Remarkably, this mechanism is homoplastic with the evolution of the C4-associated CA in the dicotyledonous genus Flaveria, although the actual mutations in the two lineages differ.

PMID:
28153918
PMCID:
PMC5338660
DOI:
10.1104/pp.16.01893
[Indexed for MEDLINE]
Free PMC Article

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