Abstract
C4 photosynthesis has evolved repeatedly from the ancestral C3 state to generate a carbon concentrating mechanism that increases photosynthetic efficiency. This specialized form of photosynthesis is particularly common in the PACMAD clade of grasses, and is used by many of the world’s most productive crops. The C4 cycle is accomplished through cell-type-specific accumulation of enzymes but cis-elements and transcription factors controlling C4 photosynthesis remain largely unknown. Using the NADP-Malic Enzyme (NADP-ME) gene as a model we tested whether mechanisms impacting on transcription in C4 plants evolved from ancestral components found in C3 species. Two basic Helix-Loop-Helix (bHLH) transcription factors, ZmbHLH128 and ZmbHLH129, were shown to bind the C4NADP-ME promoter from maize. These proteins form heterodimers and ZmbHLH129 impairs trans-activation by ZmbHLH128. Electrophoretic mobility shift assays indicate that a pair of cis-elements separated by a seven base pair spacer synergistically bind either ZmbHLH128 or ZmbHLH129. This pair of cis-elements is found in both C3 and C4 Panicoid grass species of the PACMAD clade. Our analysis is consistent with this cis-element pair originating from a single motif present in the ancestral C3 state. We conclude that C4 photosynthesis has co-opted an ancient C3 regulatory code built on G-box recognition by bHLH to regulate the NADP-ME gene. More broadly, our findings also contribute to the understanding of gene regulatory networks controlling C4 photosynthesis.
Highlights
C3 plants inherited a carbon fixation system developed by photosynthetic bacteria, with atmospheric carbon dioxide (CO2) being incorporated into ribulose-1,5bisphosphate (RuBP) by the enzyme Ribulose Bisphosphate Carboxylase/Oxygenase (RuBisCO) to form the three-carbon compound (C3) 3phosphoglycerate (Calvin and Massini 1952)
To identify transcription factors (TF) that interact with the ZmC4-NADP-Malic Enzyme (NADP-ME) gene (GRMZM2G085019), we studied the promoter region comprising 1982 base pairs upstream of the translational start site
We showed that ZmbHLH128 and ZmbHLH129 form a maize homeolog pair resulting from the recent maize whole genome duplication (WGD) event that occurred 5-12 million years ago
Summary
C3 plants inherited a carbon fixation system developed by photosynthetic bacteria, with atmospheric carbon dioxide (CO2) being incorporated into ribulose-1,5bisphosphate (RuBP) by the enzyme Ribulose Bisphosphate Carboxylase/Oxygenase (RuBisCO) to form the three-carbon compound (C3) 3phosphoglycerate (Calvin and Massini 1952). The oxygenase reaction of RuBisCO becomes more common as temperature increases and so in C3 plants photorespiration can reduce photosynthetic output by up to 30% (Ehleringer and Monson 1993). In environments such as the tropics where rates of photorespiration are high, C4 photosynthesis has evolved repeatedly from the ancestral C3 state (Lloyd and Farquhar 1994; Osborne and Beerling 2006). The ability of the C4 cycle to concentrate CO2 around RuBisCO limits oxygenation and so increases photosynthetic efficiency in conditions where photorespiration is enhanced (Hatch and Slack 1966; Maier et al 2011; Christin and Osborne 2014; Lundgren and Christin 2016)
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