Efficient Regulation of CO2 Assimilation Enables Greater Resilience to High Temperature and Drought in Maize

Increasing temperatures and extended drought episodes are among the major constraints affecting food production. Maize has a relatively high temperature optimum for photosynthesis compared to C3 crops, however, the response of this important C4 crop to the combination of heat and drought stress is p...

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Main Authors: Pedro M. P. Correia, Anabela Bernardes da Silva, Margarida Vaz, Elizabete Carmo-Silva, Jorge Marques da Silva
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.675546/full
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author Pedro M. P. Correia
Anabela Bernardes da Silva
Anabela Bernardes da Silva
Margarida Vaz
Elizabete Carmo-Silva
Jorge Marques da Silva
Jorge Marques da Silva
author_facet Pedro M. P. Correia
Anabela Bernardes da Silva
Anabela Bernardes da Silva
Margarida Vaz
Elizabete Carmo-Silva
Jorge Marques da Silva
Jorge Marques da Silva
author_sort Pedro M. P. Correia
collection DOAJ
description Increasing temperatures and extended drought episodes are among the major constraints affecting food production. Maize has a relatively high temperature optimum for photosynthesis compared to C3 crops, however, the response of this important C4 crop to the combination of heat and drought stress is poorly understood. Here, we hypothesized that resilience to high temperature combined with water deficit (WD) would require efficient regulation of the photosynthetic traits of maize, including the C4–CO2 concentrating mechanism (CCM). Two genotypes of maize with contrasting levels of drought and heat tolerance, B73 and P0023, were acclimatized at high temperature (38°C versus 25°C) under well-watered (WW) or WD conditions. The photosynthetic performance was evaluated by gas exchange and chlorophyll a fluorescence, and in vitro activities of key enzymes for carboxylation (phosphoenolpyruvate carboxylase), decarboxylation (NADP-malic enzyme), and carbon fixation (Rubisco). Both genotypes successfully acclimatized to the high temperature, although with different mechanisms: while B73 maintained the photosynthetic rates by increasing stomatal conductance (gs), P0023 maintained gs and showed limited transpiration. When WD was experienced in combination with high temperatures, limited transpiration allowed water-savings and acted as a drought stress avoidance mechanism. The photosynthetic efficiency in P0023 was sustained by higher phosphorylated PEPC and electron transport rate (ETR) near vascular tissues, supplying chemical energy for an effective CCM. These results suggest that the key traits for drought and heat tolerance in maize are limited transpiration rate, allied with a synchronized regulation of the carbon assimilation metabolism. These findings can be exploited in future breeding efforts aimed at improving maize resilience to climate change.
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spelling doaj.art-19008020f1bb4c898b4b8fa6c9c2dc022022-12-21T18:56:21ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-07-011210.3389/fpls.2021.675546675546Efficient Regulation of CO2 Assimilation Enables Greater Resilience to High Temperature and Drought in MaizePedro M. P. Correia0Anabela Bernardes da Silva1Anabela Bernardes da Silva2Margarida Vaz3Elizabete Carmo-Silva4Jorge Marques da Silva5Jorge Marques da Silva6Biosystems and Integrative Sciences Institute (BioISI), Faculdade de Ciências da Universidade de Lisboa, Lisbon, PortugalBiosystems and Integrative Sciences Institute (BioISI), Faculdade de Ciências da Universidade de Lisboa, Lisbon, PortugalDepartamento de Biologia Vegetal, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalDepartamento de Biologia, Mediterranean Institute for Agriculture (MED), Environment and Development, Universidade de Évora, Évora, PortugalLancaster Environment Centre, Lancaster University, Lancaster, United KingdomBiosystems and Integrative Sciences Institute (BioISI), Faculdade de Ciências da Universidade de Lisboa, Lisbon, PortugalDepartamento de Biologia Vegetal, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalIncreasing temperatures and extended drought episodes are among the major constraints affecting food production. Maize has a relatively high temperature optimum for photosynthesis compared to C3 crops, however, the response of this important C4 crop to the combination of heat and drought stress is poorly understood. Here, we hypothesized that resilience to high temperature combined with water deficit (WD) would require efficient regulation of the photosynthetic traits of maize, including the C4–CO2 concentrating mechanism (CCM). Two genotypes of maize with contrasting levels of drought and heat tolerance, B73 and P0023, were acclimatized at high temperature (38°C versus 25°C) under well-watered (WW) or WD conditions. The photosynthetic performance was evaluated by gas exchange and chlorophyll a fluorescence, and in vitro activities of key enzymes for carboxylation (phosphoenolpyruvate carboxylase), decarboxylation (NADP-malic enzyme), and carbon fixation (Rubisco). Both genotypes successfully acclimatized to the high temperature, although with different mechanisms: while B73 maintained the photosynthetic rates by increasing stomatal conductance (gs), P0023 maintained gs and showed limited transpiration. When WD was experienced in combination with high temperatures, limited transpiration allowed water-savings and acted as a drought stress avoidance mechanism. The photosynthetic efficiency in P0023 was sustained by higher phosphorylated PEPC and electron transport rate (ETR) near vascular tissues, supplying chemical energy for an effective CCM. These results suggest that the key traits for drought and heat tolerance in maize are limited transpiration rate, allied with a synchronized regulation of the carbon assimilation metabolism. These findings can be exploited in future breeding efforts aimed at improving maize resilience to climate change.https://www.frontiersin.org/articles/10.3389/fpls.2021.675546/fullcrop improvementdrought tolerancefood securitymaizeglobal warmingheat tolerance
spellingShingle Pedro M. P. Correia
Anabela Bernardes da Silva
Anabela Bernardes da Silva
Margarida Vaz
Elizabete Carmo-Silva
Jorge Marques da Silva
Jorge Marques da Silva
Efficient Regulation of CO2 Assimilation Enables Greater Resilience to High Temperature and Drought in Maize
Frontiers in Plant Science
crop improvement
drought tolerance
food security
maize
global warming
heat tolerance
title Efficient Regulation of CO2 Assimilation Enables Greater Resilience to High Temperature and Drought in Maize
title_full Efficient Regulation of CO2 Assimilation Enables Greater Resilience to High Temperature and Drought in Maize
title_fullStr Efficient Regulation of CO2 Assimilation Enables Greater Resilience to High Temperature and Drought in Maize
title_full_unstemmed Efficient Regulation of CO2 Assimilation Enables Greater Resilience to High Temperature and Drought in Maize
title_short Efficient Regulation of CO2 Assimilation Enables Greater Resilience to High Temperature and Drought in Maize
title_sort efficient regulation of co2 assimilation enables greater resilience to high temperature and drought in maize
topic crop improvement
drought tolerance
food security
maize
global warming
heat tolerance
url https://www.frontiersin.org/articles/10.3389/fpls.2021.675546/full
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