C3-C4 intermediacy in grasses: organelle enrichment and distribution, glycine decarboxylase expression, and the rise of C2 photosynthesis.

Roxana Khoshravesh,Tammy L Sage,Corey R Stinson,Matt Stata,Rowan F Sage,Martha Ludwig,Florian A Busch

doi:10.1093/jxb/erw150

Roxana Khoshravesh, Tammy L Sage + Show 5 more

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https://doi.org/10.1093/jxb/erw150

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Abstract

Photorespiratory glycine shuttling and decarboxylation in bundle sheath (BS) cells exhibited by C2 species is proposed to be the evolutionary bridge to C4 photosynthesis in eudicots. To evaluate this in grasses, we compare anatomy, cellular localization of glycine decarboxylase (GDC), and photosynthetic physiology of a suspected C2 grass, Homolepis aturensis, with these traits in known C2 grasses, Neurachne minor and Steinchisma hians, and C3 S laxum that is sister to S hians We also use publicly available genome and RNA-sequencing data to examine the evolution of GDC subunits and enhance our understanding of the evolution of BS-specific GDC expression in C2 and C4 grasses. Our results confirm the identity of H aturensis as a C2 species; GDC is confined predominantly to the organelle-enriched BS cells in H aturensis and S hians and to mestome sheath cells of N minor Phylogenetic analyses and data obtained from immunodetection of the P-subunit of GDC are consistent with the hypothesis that the BS dominant levels of GDC in C2 and C4 species are due to changes in expression of a single GLDP gene in M and BS cells. All BS mitochondria and peroxisomes and most chloroplasts in H aturensis and S hians are situated centripetally in a pattern identical to C2 eudicots. In S laxum, which has C3-like gas exchange patterns, mitochondria and peroxisomes are positioned centripetally as they are in S hians This subcellular phenotype, also present in eudicots, is posited to initiate a facilitation cascade leading to C2 and C4 photosynthesis.

Highlights

C4 photosynthesis has independently evolved >60 times in angiosperms (R.F. Sage et al, 2011; Grass Phylogeny Working Group II, 2012)
Plants of Homolepis aturensis Chase., Steinchisma hians Raf., and S. laxum (Sw.) Zuloaga obtained from sources described in Supplementary Table S1 at JXB online were grown at the University of Toronto in a greenhouse in 10–20 liter pots of a sandy-loam soil and were watered daily to avoid water stress
We demonstrate that the mestome sheath cells in the C2 species N. minor are functionally similar to the C2 bundle sheath (BS) cells of H. aturensis and S. hians because glycine decarboxylase (GDC) is almost exclusively located in organelle-enriched mestome sheath cells in the high vein density leaves

Summary

Introduction

C4 photosynthesis has independently evolved >60 times in angiosperms (R.F. Sage et al, 2011; Grass Phylogeny Working Group II, 2012). C4 photosynthesis has independently evolved >60 times in angiosperms Sage et al, 2011; Grass Phylogeny Working Group II, 2012). The Poaceae represents the most prolific family of C4 origins, with approximately twice as many origins as any other family (Sage, 2016). C4 grasses make up the greatest number of C4 species, comprising ~60% of the 8000 estimated number of C4 species (Still et al, 2003; Sage, 2016). A quarter of global net primary productivity on land is due to C4 photosynthesis (Still et al, 2003), of which the vast majority is contributed by grasses (Sage et al, 1999). C4 grasses have great significance for humanity as they dominate the fraction of biomass entering the human food chain as grain (maize, sorghum, and millets), sugar (sugarcane), and fodder for animals, and

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