Abstract
C4 photosynthesis is an adaptive photosynthetic pathway which concentrates CO2 around Rubisco in specialized bundle sheath cells to reduce photorespiration. Historically, the pathway has been characterized into three different subtypes based on the decarboxylase involved, although recent work has provided evidence that some plants can use multiple decarboxylases, with maize in particular using both the NADP-malic enzyme (NADP-ME) pathway and phosphoenolpyruvate carboxykinase (PEPCK) pathway. Parallel C4 pathways could be advantageous in balancing energy and reducing equivalents between bundle sheath and mesophyll cells, in decreasing the size of the metabolite gradients between cells and may better accommodate changing environmental conditions or source to sink demands on growth. The enzyme activity of C4 decarboxylases can fluctuate with different stages of leaf development, but it remains unclear if the pathway flexibility is an innate aspect of leaf development or an adaptation to the leaf microenvironment that is regulated by the plant. In this study, variation in the two C4 pathways in maize were characterized at nine plant ages throughout the life cycle. Two positions in the canopy were examined for variation in physiology, gene expression, metabolite concentration, and enzyme activity, with particular interest in asparagine as a potential regulator of C4 decarboxylase activity. Variation in C4 and C3 metabolism was observed for both leaf age and canopy position, reflecting the ability of C4 pathways to adapt to changing microenvironments.
One Sentence Summary The proportion of the two C4 pathways in maize plants is dependent on canopy position and not the age of the leaf.
Footnotes
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Funding Sources: Funding for the research was provided by the National Science Foundation Plant Genome Research Program (PGRP) postdoctoral fellowship (NSF-1812235) to J.A., and PGRP Award IOS-1829365, the United States Department of Agriculture National Institute of Food and Agriculture (2017-67013-26156; 2016-67013-24585), the Office of Biological and Environmental Research in the DOE Office of Science (DE-SC0008769), and the National Institutes of Health (U01 CA235508). Support was also provided by United States Department of Agriculture Agricultural Research Service. Support for the acquisition of the 6500 QTRAP LC–MS/MS was provided by the National Science Foundation (DBI #1427621).