Photosynthetic flexibility in maize exposed to salinity and shade

Abstract

C4 photosynthesis involves a close collaboration of the C 3 and C4 metabolic cycles across the mesophyll and bundlesheath cells. This study investigated the coordination of C4 photosynthesis in maize plants subjected to two salinity (50 and 100 mM NaCl) treatments and one shade (20% of full sunlight) treatment. Photosynthetic efficiency was probed by combining leaf gas-exchange measurements with carbon isotope discrimination and assaying the key carboxylases [ribulose-1,5- bisphosphate carboxylase/oxygenase (Rubisco) and phosphoenolpyruvate carboxylase (PEPC)] and decarboxylases [nicotinamide adenine dinucleotide phosphate malic enzyme (NADP-ME) and phosphoenolpyruvate carboxykinase (PEP-CK)] operating in maize leaves. Generally, salinity inhibited plant growth and photosynthesis to a lesser extent than shade. Salinity reduced photosynthesis primarily by reducing stomatal conductance and secondarily by equally reducing Rubisco and PEPC activities; the decarboxylases were inhibited more than the carboxylases. Salinity increased photosynthetic carbon isotope discrimination (δp) and reduced leaf dry-matter carbon isotope composition (13δ) due to changes in pi/pa (intercellular to ambient CO 2 partial pressure), while CO2 leakiness out of the bundle sheath (θ) was similar to that in control plants. Acclimation to shade was underpinned by a greater downregulation of PEPC relative to Rubisco activity, and a lesser inhibition of NADP-ME (primary decarboxylase) relative to PEP-CK (secondary decarboxylase). Shade reduced δp and without significantly affecting leaf 13δ or pi/pa relative to control plants. Accordingly, shade perturbed the balance between the C3 and C4 cycles during photosynthesis in maize, and demonstrated the flexible partitioning of C4 acid decarboxylation activity between NADP-ME and PEP-CK in response to the environment. This study highlights the need to improve our understanding of the links between leaf 13δ and photosynthetic δp, and the role of the secondary decarboxylase PEP-CK in NADP-ME plants such as maize.