Lack of mitochondrial thioredoxin o1 is compensated by antioxidant components under salinity in Arabidopsis thaliana plants

Abstract

In a changing environment, plants are able to acclimate to new conditions by regulating their metabolism through the antioxidant and redox systems involved in the stress response. Here, we studied a mitochondrial thioredoxin in wild-type (WT) Arabidopis thaliana and two Attrxo1 mutant lines grown in the absence or presence of 100 mM NaCl. Compared to WT plants, no evident phenotype was observed in the mutant plants under control condition, although they had higher number of stomata, loss of water, nitric oxide and carbonyl protein contents as well as higher activity of superoxide dismutase (SOD) and catalase enzymes than WT plants. Under salinity, the mutants presented lower water loss and higher stomatal closure, H O and lipid peroxidation levels accompanied by higher enzymatic activity of catalase and the different SOD isoenzymes compared to WT plants. These inductions may collaborate in the maintenance of plant integrity and growth observed under saline conditions, possibly as a way to compensate the lack of TRXo1. We discuss the potential of TRXo1 to influence the development of the whole plant under saline conditions, which have great value for the agronomy of plants growing under unfavorable environment.

Thioredoxin Network in Plant Mitochondria: Cysteine S-Posttranslational Modifications and Stress Conditions

“…Results on the changes in secondary metabolites with a large number of metabolites increasing in at least one of the Attrxo1 mutants following two cycles of drought, reinforces the idea that secondary metabolism is redox regulated by TRX system (Figure 4). Finally, the analysis of the increased stomatal conductance following drought recovery suggested a TRXo1 redox regulation of stoma function (Figure 4) which fits well with the previously reported involvement of TRXo1 mediated redox regulation of stomatal dynamic and function under salinity (Calderoń et al, 2018b).…”

“…In this sense, loss of function trxo 1 -1 and trxo 1 -2 mutants have been used not only to corroborate a role for the TRX system in regulating different metabolic processes in mitochondria but also to define the importance of mitochondrial TRXs under stress conditions ( Daloso et al, 2015 ; Calderón et al, 2018a ). However, in these studies, no extreme phenotype has been described, either in standard or stress conditions, possibly due to the redundancy or overlapping functions with mitochondrial or cytosolic proteins as other TRXs and GRXs ( Daloso et al, 2015 ; Geigenberger et al, 2017 ; Ortiz-Espín et al, 2017 ; Calderón et al, 2018a ; Calderón et al, 2018b ; Sánchez-Guerrero et al, 2019 ). The information related to the physiological mitochondrial TRX o 1/TRX h 2 function in plant stress acclimation is scarce.…”

“…Overall, the results demonstrated the participation of PsTRX o 1 as a component in the mitochondrial antioxidant response allowing plant salinity adaptation ( Martí et al, 2011 ). In order to gain further insight into the physiological and metabolic function of the mitochondrial TRX o 1 in the plant acclimation to saline stress, we have recently used two independent mitochondrial Attrxo1 mutants ( Attrxo1-1, Attrxo1-2 ) ( Calderón et al, 2018b ). Their responses to salinity fit well with those reported by Martí et al (2011) in pea plants, all pointing that TRX o 1 is required for the proper functioning of the antioxidant metabolism including compensatory mechanisms, as higher levels of H 2 O 2 and NO, an upregulation of all SOD isoforms, catalase and GR, alterations in the glutathione redox state, due to maintained GSH content in Attrxo1 plants and changes in stomatal density, stomatal closure with lower water loss, which may be also a key factor for the adaptative response to salinity ( Calderón et al, 2018b ) ( Figure 4 ).…”

“…In order to gain further insight into the physiological and metabolic function of the mitochondrial TRX o 1 in the plant acclimation to saline stress, we have recently used two independent mitochondrial Attrxo1 mutants ( Attrxo1-1, Attrxo1-2 ) ( Calderón et al, 2018b ). Their responses to salinity fit well with those reported by Martí et al (2011) in pea plants, all pointing that TRX o 1 is required for the proper functioning of the antioxidant metabolism including compensatory mechanisms, as higher levels of H 2 O 2 and NO, an upregulation of all SOD isoforms, catalase and GR, alterations in the glutathione redox state, due to maintained GSH content in Attrxo1 plants and changes in stomatal density, stomatal closure with lower water loss, which may be also a key factor for the adaptative response to salinity ( Calderón et al, 2018b ) ( Figure 4 ). At mitochondrial level, a more recent study has revealed the impact of the lack of TRX o 1 in the acclimation to salinity, with an important in vivo reorganization of the respiratory and antioxidant enzymes as well as metabolic responses ( Sánchez-Guerrero et al, 2019 ).…”

Thioredoxin h2 contributes to the redox regulation of mitochondrial photorespiratory metabolism

“…Taken together, these results contribute to elucidate an elusive question concerning whether the TRX system could also regulates the photorespiratory metabolism, as previously demonstrated for both photosynthetic and respiratory metabolism (Buchanan, ; Daloso et al, ; Gelhaye et al, ; Michalska, Zauber, Buchanan, Cejudo, & Geigenberger, ; Michelet et al, ; Schmidtmann et al, ). Given the recognized role of photorespiration (Wingler et al, ) and the TRX system for plant stress acclimation (Calderón et al, ; Fonseca‐Pereira, Daloso, Gago, Nunes‐Nesi, & Araújo, ; Fonseca‐Pereira et al, ), the extent by which this TRX‐mediated regulation of the photorespiratory metabolism influence plants stress responses assumes an importance to be further investigated.…”