Exploiting differences in the energy budget among C4 subtypes to improve crop productivity.

Xinyou Yin,Paul C Struik

doi:10.1111/nph.17011

Abstract

SummaryC4 crops of agricultural importance all belong to the NADP‐malic enzyme (ME) subtype, and this subtype has been the template for C4 introductions into C3 crops, like rice, to improve their productivity. However, the ATP cost for the C4 cycle in both NADP‐ME and NAD‐ME subtypes accounts for > 40% of the total ATP requirement for CO2 assimilation. These high ATP costs, and the associated need for intense cyclic electron transport and low intrinsic quantum yield ΦCO2, are major constraints in realizing strong improvements of canopy photosynthesis and crop productivity. Based on mathematical modelling, we propose a C4 ideotype that utilizes low chloroplastic ATP requirements present in the nondomesticated phosphoenolpyruvate carboxykinase (PEP‐CK) subtype. The ideotype is a mixed form of NAD(P)‐ME and PEP‐CK types, requires no cyclic electron transport under low irradiances, and its theoretical ΦCO2 is c. 25% higher than that of a C4 crop type. Its cell‐type‐specific ATP and NADPH requirements can be fulfilled by local energy production. The ideotype is projected to have c. 10% yield advantage over NADP‐ME‐type crops and > 50% advantage over C3 counterparts. The ideotype provides a unique (theoretical) case where ΦCO2 could be improved, thereby paving a new avenue for improving photosynthesis in both C3 and C4 crops.

Highlights

Increasing yields of major food crops, like wheat and rice, to cope with increasing populations is a major challenge in agriculture, especially in the face of an accelerating climate change (Fischer et al, 2014)
More recent analysis, using a crop model based on more detailed physiological parameters, showed that potential productivity of rice when grown under the current climatic condition could be increased by only 33–42% by introducing the complete maize-like C4 mechanism, and the advantage was even lower under future high-CO2 atmospheric conditions (Yin & Struik, 2017)
0.17 x, the proportion of the chloroplastic ATP that is used to support the C4 or CO2-concentrating mechanism cycle; na, not applicable. n, stoichiometric coefficient for the number of ATP generated per NADH oxidation; fCET, ΦCO2, and x in the last three columns were estimated assuming that all C4 types had the same leakiness (0.16; Yin & Struik, 2012) and the same proportions for alternative energy sinks, to allow objective comparison of their intrinsic quantum yield. aThe word ‘Minimum’ is used because data in these columns do not include energy loss due to leakiness and energy requirements by alternative energy sinks. bNADPH and ATP requirements for these types are derived from discussion in the text; fCET, fraction for cyclic electron transport

Summary

C4 crops of agricultural importance all belong to the NADP-malic enzyme (ME) subtype, and this subtype has been the template for C4 introductions into C3 crops, like rice, to improve their productivity. The ATP cost for the C4 cycle in both NADP-ME and NAD-ME subtypes accounts for > 40% of the total ATP requirement for CO2 assimilation. These high ATP costs, and the associated need for intense cyclic electron transport and low intrinsic quantum yield ΦCO2 , are major constraints in realizing strong improvements of canopy photosynthesis and crop productivity. The ideotype is a mixed form of NAD(P)-ME and PEP-CK types, requires no cyclic electron transport under low irradiances, and its theoretical ΦCO2 is c. The ideotype provides a unique (theoretical) case where ΦCO2 could be improved, thereby paving a new avenue for improving photosynthesis in both C3 and C4 crops

Introduction

ATP fCET

Fraction of PSI in BS

Concluding remarks

Findings

Supporting Information