TY - JOUR
T1 - Cold stress-induced changes in metabolism of carbonyl compounds and membrane fatty acid composition in chickpea
AU - Javidi, Mohammad Reza
AU - Maali-Amiri, Reza
AU - Poormazaheri, Helen
AU - Sadeghi Niaraki, Mina
AU - Kariman, Khalil
N1 - Funding Information:
Along with non-enzymatic compounds such as ROS, MDA (as the oxidized product of UFAs) may also be generated by enzymatic LOX activity in plant cells (Berger et al., 2001; Lopes et al., 2011). Therefore, the MDA content can be influenced by activity of LOX under CS conditions. In the tolerant and the sensitive genotypes, the LOX activity showed a significant upsurge (by 4.69- and 2.55-fold, respectively) at 6 DAS (Fig. 3a and b). On the other hand, the LOX activity was statistically higher in the sensitive plants compared to the tolerant ones at 1 DAS (2.17-fold), 3 DAS (1.6-fold) and 6 DAS (2.4-fold), respectively (Fig. 3a and b). The increased LOX activity has been attributed to enhanced lipid peroxidation and also biosynthesis of oxylipins (particularly, C6-volatile compounds and jasmonates) with signaling roles (Mano et al., 2019; Viswanath et al., 2020). Based on our results, the change patterns of MDA and LOX activity revealed reciprocal relationships in chickpea genotypes exposed to CS. In early stage of CS, the MDA content and LOX activity significantly increased in both genotypes, whereas they showed the opposite trend during the late stage (at 6 DAS) in the tolerant genotype (Fig. 1b; Fig. 3 a,b). Therefore, the MDA content is related to the ROS accumulation, instead of LOX activity at 6 DAS, which is in line with the change patterns of H2O2 content. However, in early stages of CS, the change patterns of MDA content were consistent with the H2O2 content and LOX activity. This is related to mutual efforts of LOX activity during short-term and long-term CS conditions in chickpea. Interestingly, in cold-tolerant genotype, the maximum activity of the LOX enzyme occurred along with minimum values of H2O2 and MDA contents, suggesting that the LOX activity may not represent a direct relationship with cellular damages during CS. Significant increases in DBI and UFAs were observed during late stages of CS in the tolerant genotype, when the H2O2 and MDA contents showed the lowest values (Fig. 1a and b; Fig. 2a; Fig. 3a). This means that the relative increase of LOX activity can act as an important factor for cold tolerance development in the tolerant genotype through inducing the plant defense systems (Wang et al., 2009; Liu et al., 2016). In the sensitive genotype, however, the severe changes of LOX activity induce cell membrane damages and possibly cell death (confirmed by MDA and H2O2 results) during CS (Fig. 1a and b; Fig. 3b). Therefore, protecting membrane structure and function can be considered as a vital strategy of plant cells under CS conditions, which can be comprehended via balanced activity of LOX in chickpea. Thus, under severe stresses, the decreased activity of LOX may be compensated by other signaling components such as ABA and salicylic acid through adjusting the cellular metabolism and inducing defense systems (Bhardwaj et al., 2011; Montillet et al., 2013). However, in early responses, the relative increase in LOX activity was accompanied by H2O2 and MDA accumulations, suggesting its potential role in production of oxidative products and signaling molecules as main stimulators of regulatory and defense machinery (when a relative increase in MDA content does not mean a cellular damage yet). Such hypothesis can be partly supported by the lack of increase in antioxidative activities during the early responses of both genotypes to CS as we documented previously (Karami-Moalem et al., 2018). Therefore, such inconsistencies may be a result of upstream regulatory reactions, which induce tolerance responses, particularly in the tolerant genotype. Overexpression of LOX in plants has shown tolerance responses to environmental stresses through decreasing the accumulation of H2O2 and lipid peroxidation, and upregulation of defense genes (Hou et al., 2015; Kotapati et al., 2017). In the tolerant genotype, the decrease in DBI index in early responses occurred due to the initial increase in H2O2, MDA, and LOX activity while in late responses, the DBI increased despite a gradual but limited increase in LOX activity (Fig. 3a). Several studies have shown that higher DBI is related to the increased activity of desaturase enzymes, which introduce double bonds in FA components of lipids (Los and Murata, 2004; Maali-Amiri et al., 2010). This is conforming to the UFAs content as well as the regulated activity of LOX at 6 DAS. Increased DBI was one of the early responses in the sensitive genotype, however, in late responses, the DBI index decreased along with a continuous increase in LOX activity (Fig. 3b). Accordingly, the late responses tended to show greater significance for cold tolerance development in chickpea. Based on our results, it can be concluded that the understanding of stress tolerance mechanisms in chickpea requires in-depth knowledge of regulatory mechanisms, defense machinery, along with modulation of damage indices.This work was supported, in part, by Grants from University of Tehran, Iran.
Funding Information:
This work was supported, in part, by Grants from University of Tehran, Iran .
Publisher Copyright:
© 2022
PY - 2022/12/1
Y1 - 2022/12/1
N2 - In this study, changes in membrane fatty acid (FA) composition and damage indices contents as well as the transcript patterns of carbonyl-detoxifying genes were evaluated in two chickpea (Cicer arietinum L.) genotypes, cold-tolerant Sel96th11439 and cold-sensitive ILC533 under cold stress (CS; 4 °C). During CS, H2O2 and malondialdehyde (MDA) contents increased (by 47% and 57%, respectively) in the sensitive genotype, while these contents remained unchanged in the tolerant genotype. In tolerant plants, higher content of linoleic, linolenic, unsaturated FAs (UFAs), total FAs and double bond index (DBI) (by 23, 21, 19, 17 and 9%, respectively) was observed at 6 days after stress (DAS) compared to sensitive plants, which, along with alterations of the damage indices, indicate their enhanced tolerance to CS. Compared with the sensitive genotype, less lipoxygenase (LOX) activity (by 59%) in the tolerant genotype was accompanied by decreased MDA and increased levels of UFAs and DBI during CS, particularly at 6 DAS. Upregulation of aldehyde dehydrogenase and aldo-keto reductase genes (by 9- and 10-fold, respectively) at 1 DAS, along with the enhanced transcript levels of aldehyde reductase and 2-alkenal reductase (by 3- and 14.7-fold, respectively) at 6 DAS were accompanied by increased UFAs and reduced MDA contents in the tolerant genotype. Overall, the results suggest that cold tolerance in chickpea was partly associated with regulation of membrane FA compositions and the potential metabolic networks involved in synthesis and degradation of carbonyl compounds.
AB - In this study, changes in membrane fatty acid (FA) composition and damage indices contents as well as the transcript patterns of carbonyl-detoxifying genes were evaluated in two chickpea (Cicer arietinum L.) genotypes, cold-tolerant Sel96th11439 and cold-sensitive ILC533 under cold stress (CS; 4 °C). During CS, H2O2 and malondialdehyde (MDA) contents increased (by 47% and 57%, respectively) in the sensitive genotype, while these contents remained unchanged in the tolerant genotype. In tolerant plants, higher content of linoleic, linolenic, unsaturated FAs (UFAs), total FAs and double bond index (DBI) (by 23, 21, 19, 17 and 9%, respectively) was observed at 6 days after stress (DAS) compared to sensitive plants, which, along with alterations of the damage indices, indicate their enhanced tolerance to CS. Compared with the sensitive genotype, less lipoxygenase (LOX) activity (by 59%) in the tolerant genotype was accompanied by decreased MDA and increased levels of UFAs and DBI during CS, particularly at 6 DAS. Upregulation of aldehyde dehydrogenase and aldo-keto reductase genes (by 9- and 10-fold, respectively) at 1 DAS, along with the enhanced transcript levels of aldehyde reductase and 2-alkenal reductase (by 3- and 14.7-fold, respectively) at 6 DAS were accompanied by increased UFAs and reduced MDA contents in the tolerant genotype. Overall, the results suggest that cold tolerance in chickpea was partly associated with regulation of membrane FA compositions and the potential metabolic networks involved in synthesis and degradation of carbonyl compounds.
KW - Carbonyl
KW - Chickpea
KW - Cold responses
KW - Gene expression
KW - Lipid peroxidation
KW - Membrane fatty acids
UR - http://www.scopus.com/inward/record.url?scp=85139278113&partnerID=8YFLogxK
U2 - 10.1016/j.plaphy.2022.09.031
DO - 10.1016/j.plaphy.2022.09.031
M3 - Article
C2 - 36201983
AN - SCOPUS:85139278113
VL - 192
SP - 10
EP - 19
JO - Plant physiology and biochemistry : PPB
JF - Plant physiology and biochemistry : PPB
SN - 0981-9428
ER -