Exogenous Calcium Alleviates Nocturnal Chilling-Induced Feedback Inhibition of Photosynthesis by Improving Sink Demand in Peanut (Arachis hypogaea)

Abstract

Arachis hypogaea (peanut) is a globally important oilseed crop with high nutritional value. However, upon exposure to overnight chilling stress, it shows poor growth and seedling necrosis in many cultivation areas worldwide. Calcium (Ca2+) enhances chilling resistance in various plant species. We undertook a pot experiment to investigate the effects of exogenous Ca2+ and a calmodulin (CaM) inhibitor on growth and photosynthetic characteristics of peanut exposed to low night temperature (LNT) stress following warm sunny days. The LNT stress reduced growth, leaf extension, biomass accumulation, gas exchange rates, and photosynthetic electron transport rates. Following LNT stress, we observed larger starch grains and a concomitant increase in nonstructural carbohydrates and hydrogen peroxide (H2O2) concentrations. The LNT stress further induced photoinhibition and caused structural damage to the chloroplast grana. Exogenous Ca2+ enhanced plant growth following LNT stress, possibly by allowing continued export of carbohydrates from leaves. Foliar Ca2+ likely alleviated the nocturnal chilling-dependent feedback limitation on photosynthesis in the daytime by increasing sink demand. The foliar Ca2+ pretreatment protected the photosystems from photoinhibition by facilitating cyclic electron flow (CEF) and decreasing the proton gradient (ΔpH) across thylakoid membranes during LNT stress. Foliar application of a CaM inhibitor increased the negative impact of LNT stress on photosynthetic processes, confirming that Ca2+–CaM played an important role in alleviating photosynthetic inhibition due to the overnight chilling-dependent feedback.

Integrated Transcriptomics and Metabolomics Analysis Reveal Key Metabolism Pathways Contributing to Cold Tolerance in Peanut

“…Cold weather accounts for serious reductions in crop yield every year, since many agriculturally important crops, including rice ( Oryza sativa ) and peanut, are chilling sensitive and can only be cultivated in tropical or subtropical regions ( Wu et al, 2020 ). Despite the molecular mechanisms of cold-induced reprogramming of gene expression and the metabolite accumulation pattern were extensively studied in model plants ( Hoermiller et al, 2016 ; Jin et al, 2017 ; Pagter et al, 2017 ; Dasgupta et al, 2020 ), only a handful of reports were related to peanut ( Jiang et al, 2020 ; Wu et al, 2020 ; Zhang H. et al, 2020 ). In this study, we attempted to decipher the regulatory mechanisms of peanut in response to cold stress through combining transcriptome with metabolome analysis.…”

The Physiological Functionality of PGR5/PGRL1-Dependent Cyclic Electron Transport in Sustaining Photosynthesis

“…This is the PSI donor-side regulation by CET for PSI photoprotection ( Suorsa et al, 2012 ). It has been reported that exogenous calcium alleviates nocturnal chilling-induced photo damage by facilitating CET, thereby enhancing the photosynthesis and biomass accumulation of peanut under low nocturnal temperature stress ( Song et al, 2020 ; Wu et al, 2020 ). Additionally, plant dry weight was significantly lowered in the rice PGR 5-knockdown line compared to that of WT, especially under fluctuating light ( Yamori et al, 2016 ).…”

“…The bulk of our earth's energy resources is derived from global photosynthetic activity in either recent or ancient times (Vass et al, 2007;Liu et al, 2011;Lambers and Oliveira, 2019;Nawrocki et al, 2019). The normal operation of photosynthesis is inseparable from the participation of light energy, but any excessive high light would impact the photosystem II (PSII), photosystem I (PSI) and the other thylakoid membrane proteins and resulting in photoinhibition and the accumulation of reactive oxygen species (ROS; Foyer and Noctor, 1999;Chaux et al, 2017;Liu, 2020). In the real world, multiple stress episodes affecting growth and development are common (Suzuki et al, 2014).…”

“…In the real world, multiple stress episodes affecting growth and development are common ( Suzuki et al, 2014 ). Any excessive high light situation could be exacerbated further with a co-occurring high temperature ( Sun et al, 2017 ; Lu et al, 2020 ), low temperature ( Liu et al, 2013 ; Song et al, 2020 ; Wu et al, 2020 ), phosphorus deficiency ( Carstensen et al, 2018 ; Shi et al, 2019 ) and drought ( Wada et al, 2019 ). Plants have evolved several adaptations to cope with the unfavorable light situation: adjusting leaf orientation, ROS scavenging competence ( Gill and Tuteja, 2010 ), xanthophyll cycle ( Kuczynska et al, 2020 ), state transitions strategy ( Hepworth et al, 2021 ), cyclic electron transport (CET; Yadav et al, 2020 ) and photorespiration ( Storti et al, 2019 ).…”

The Significance of Chloroplast NAD(P)H Dehydrogenase Complex and Its Dependent Cyclic Electron Transport in Photosynthesis

“…Under saturated light, CET provides an important photoprotective role for the activity of oxygen evolution complex (OEC) by forming the proton gradient across the thylakoid membrane (?pH) (Huang et al, 2016b), and pmf to protect PSI and PSII via the acidification of thylakoid lumen (Golding et al, 2004;Basso et al, 2020). Chilling leads to photoinhibition in cold-sensitive plants like tobacco, peanut, and cucumber which is mainly related to CET activity (Huang et al, 2016a;Liu, 2020;Song et al, 2020;Wu et al, 2020). At 4 • C, CET plays a photoprotective role in PSI primarily through the acidification of thylakoid lumen (Huang et al, 2017b).…”