C₃–C₄intermediacy in grasses: organelle enrichment and distribution, glycine decarboxylase expression, and the rise of C₂photosynthesis

Abstract

HighlightC2 photosynthesis in grasses is facilitated by organelle enrichment in tandem with enhanced levels of GDC in the carbon-concentrating cells consistent with changes in expression of a single GLDP gene.

The Evolutionary Origin of C4 Photosynthesis in the Grass Subtribe Neurachninae

“…Together with physiological and biochemical investigations, these studies support the hypothesis of Monson et al (1984) that the C 4 pathway arose via a series of innovations that initially enabled plants to refix a large fraction of photorespired CO 2 via the shuttling of Gly from the mesophyll (M) to a sheath of cells surrounding the vascular tissue, where the Gly is decarboxylated (for review, see Sage et al, 2014). The sheath layer is most commonly the bundle sheath (BS) cells, although in some grasses the mestome sheath (MS) cells is where decarboxylation of Gly occurs (Khoshravesh et al, 2016). Associated with the shuttling of Gly is a shift in the expression of the mitochondrial enzyme Gly decarboxylase (GDC) from M cells to the vascular sheath tissue.…”

“…An important early step proposed for C 2 evolution is the physiological activation of the BS of C 3 species (Gowik and Westhoff, 2011;Sage et al, 2014). Activation of the BS is facilitated by increases in the number and size of mitochondria and chloroplasts and repositioning of mitochondria plus a few chloroplasts to the centripetal pole of the BS, possibly to facilitate refixation of some photorespired CO 2 produced in the leaf (Muhaidat et al, 2011;Sage et al, 2013;Voznesenskaya et al, 2013;Khoshravesh et al, 2016). Together, organelle enrichment and repositioning have been termed the "proto-Kranz" phase of early C 4 evolution, and is recognized in close relatives of C 3 and C 2 species in the eudicot genera Flaveria, Heliotropium, and Salsola, and the monocot genus Steinchisma (Muhaidat et al, 2011;Sage et al, 2013;Khoshravesh et al, 2016;Schüssler et al, 2017).…”

“…Transition to the C 2 condition occurs with further increases in mitochondrial size and numbers in the BS, increased chloroplast numbers in the BS, and a repositioning of most chloroplasts to the centripetal wall of BS cells (Brown and Hattersley, 1989;Muhaidat et al, 2011;Sage et al, 2013;Khoshravesh et al, 2016). Increases in vein density and BS crosssectional area can occur in concert with organelle and GDC enrichment in sheath cells of proto-Kranz and C 2 species, and the size and numbers of M cells often decline as well (McKown and Dengler 2007;Muhaidat et al, 2011;Sage et al, 2013;Khoshravesh et al, 2016). Because metabolite flux between M and sheath cells increases as the C 2 and C 4 pathways evolve, increased intercellular transport capacity between these compartments should also increase.…”

“…By contrast, only a handful of C 3 -C 4 intermediate monocots are known, which is surprising given the predominance of monocot taxa among the C 4 flora. Despite accounting for 78% of all C 4 species, only four of 30 C 4 monocot lineages are known to have C 3 -C 4 intermediate species (Hattersley and Stone, 1986;Khoshravesh et al, 2016;Lundgren et al, 2016;Sage, 2016). Of these, the grass genera Alloteropsis and Neurachne also contain C 4 species, but have only one recognized intermediate species each; Steinchisma has five or six species exhibiting C 2 photosynthesis, but it is not close to any C 4 clade (Brown et al, 1983;Aliscioni et al, 2003;Grass Phylogeny Working Group II, 2012).…”

“…The above considerations indicate that identification of additional C 3 -C 4 intermediates in grasses and sedges would promote understanding of C 4 evolution in the monocots. To this end, C 3 -C 4 intermediates in the grass genera Alloteropsis and Homolepis have been recently identified (Khoshravesh et al, 2016;Lundgren et al, 2016). Another approach is to re-examine the grass genus Neurachne and its allies in the subtribe Neurachninae, where work in the 1980s identified one C 2 species (Neurachne minor), two C 4 species (Neurachne munroi, and Neurachne muelleri-formerly Paraneurachne muelleri), and four putative C 3 species (Neurachne alopecuroidea, Neurachne lanigera, Neurachne queenslandica, Neurachne tenuifolia; Hattersley et al, 1982Hattersley and Roksandic, 1983;Hattersley and Stone, 1986).…”