Maize metabolome and proteome responses to controlled cold stress partly mimic early‐sowing effects in the field and differ from those of Arabidopsis

Abstract

In Northern Europe, sowing maize one-month earlier than current agricultural practices may lead to moderate chilling damage. However, studies of the metabolic responses to low, non-freezing, temperatures remain scarce. Here, geneticallydiverse maize hybrids (Zea mays, dent inbred lines crossed with a flint inbred line) were cultivated in a growth chamber at optimal temperature and then three decreasing temperatures for 2 days each, as well as in the field. Leaf metabolomic and proteomic profiles were determined. In the growth chamber, 50% of metabolites and 18% of proteins changed between 20 and 16 C. These maize responses, partly differing from those of Arabidopsis to short-term chilling, were mapped on genome-wide metabolic maps. Several metabolites and proteins showed similar variation for all temperature decreases: seven MS-based metabolite signatures and two proteins involved in photosynthesis decreased continuously. Several increasing metabolites or proteins in the growth-chamber chilling conditions showed similar trends in the early-sowing field experiment, including trans-aconitate, three hydroxycinnamate derivatives, a benzoxazinoid, a sucrose synthase, lethal leaf-spot 1 protein, an allene oxide synthase, several glutathione transferases and peroxidases. Hybrid groups based on field biomass were used to search for the metabolite or

Can we improve the chilling tolerance of maize photosynthesis through breeding?

“…Evidence for this hypothesis comes from other plant species including evergreens and Arabidopsis , in which chilling acclimation led to alterations to the thylakoid membrane, sucrose synthesis enzyme expression, and Calvin cycle enzyme expression, all of which have been identified as balancing regulators of the carbon source and sink enabling photosynthetic acclimation to chilling stress ( Hüner et al ., 1998 , 2003 ; Stitt and Hurry, 2002 ). In maize, expression of a sucrose synthase increased in response to chilling stress ( Urrutia et al , 2021 ), as has been seen in Arabidopsis ( Stitt and Hurry, 2002 ), and down-regulation of the expression of photosynthetic enzymes is also observed, as we outline in the following section.…”

“…Decreases in F v / F m were also reported at 2, 4, and 8 h into a chilling stress period, with greater decreases observed as time progressed ( Dolstra et al , 1994 ). The down-regulation of Φ PSII has also been reported a few hours after the imposition of chilling stress ( Sobkowiak et al , 2014 ); after 1 d of chilling stress ( Sobkowiak et al ., 2014 , 2016 ), and after 2 d ( Janowiak et al , 2002 ; Sobkowiak et al , 2014 ; Urrutia et al , 2021 ), 4 d ( Urrutia et al , 2021 ), 5 d ( Sobkowiak et al , 2014 ), 6 d ( Urrutia et al , 2021 ), 8 d ( Lee et al , 2002 ), and 10 d ( Kościelniak et al , 2005 ). Each of these results was obtained during the period of chilling stress, although the study by Janowiak et al also included measurements made during a recovery period which are not reported here.…”

“…the abundance of photosynthesis-related transcripts) has been reported as early as 4 h after the beginning of chilling stress ( Li et al , 2019 ), after 12 h in another study ( Yu et al , 2021 ), and after 1 d of chilling stress in several studies ( Trzcinska-Danielewicz et al , 2009 ; Zhang et al , 2009 ; Jończyk et al , 2017 ; Avila et al , 2018 ; Banović Đeri et al , 2021 ). A decrease in photosynthetic protein accumulation occurs soon after, reported after 2 d of chilling stress ( Urrutia et al , 2021 ). This decrease may be caused by the transcriptional or translational down-regulation of photosynthetic genes leading to a reduction in protein synthesis; by the damage and breakdown of photosynthetic proteins discussed above; by damage to the cellular machinery responsible for the synthesis and repair of proteins; or by a combination of these factors.…”

Primary and Phenolic Metabolites Analyses, In Vitro Health-Relevant Bioactivity and Physical Characteristics of Purple Corn (Zea mays L.) Grown at Two Andean Geographical Locations

“…These changes in TCA cycle-derived metabolites might reflect a high mitochondrial activity with consequent generation of ATP and reducing agents as a protective mechanism to environmental abiotic stress [63]. The increase in organic acids linked to the TCA cycle has also been reported in buckwheat seedlings, and maize leaves subjected to cold treatments with variable profiles depending on the range of the temperature decrease [59,63,64].…”

Comparative Transcriptomics for Pepper (Capsicum annuum L.) under Cold Stress and after Rewarming

“…In this study, significant changes of petB (Capana01g003214) occurred only in CT cultivars. Previous studies have shown various LHC compounds involved in several chloroplast functions, including photosynthetic pigment metabolism and photosynthetic electron transport chain, to adapt cold stress [52]. The increase of LHC is beneficial to adjust the organization of photosystem II and photoprotection.…”