LSD1‐, EDS1‐ and PAD4‐dependent conditional correlation among salicylic acid, hydrogen peroxide, water use efficiency and seed yield in Arabidopsis thaliana

Abstract

In Arabidopsis thaliana, LESION SIMULATING DISEASE 1 (LSD1), ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) and PHYTOALEXIN DEFICIENT 4 (PAD4) proteins are regulators of cell death (CD) in response to abiotic and biotic stresses. Hormones, such as salicylic acid (SA), and reactive oxygen species, such as hydrogen peroxide (H2O2), are key signaling molecules involved in plant CD. The proposed mathematical models presented in this study suggest that LSD1, EDS1 and PAD4 together with SA and H2O2 are involved in the control of plant water use efficiency (WUE), vegetative growth and generative development. The analysis of Arabidopsis wild‐type and single mutants lsd1, eds1, and pad4, as well as double mutants eds1/lsd1 and pad4/lsd1, demonstrated the strong conditional correlation between SA/H2O2 and WUE that is dependent on LSD1, EDS1 and PAD4 proteins. Moreover, we found a strong correlation between the SA/H2O2 homeostasis of 4‐week‐old Arabidopsis leaves and a total seed yield of 9‐week‐old plants. Altogether, our results prove that SA and H2O2 are conditionally regulated by LSD1/EDS/PAD4 to govern WUE, biomass accumulation and seed yield. Conditional correlation and the proposed models presented in this study can be used as the starting points in the creation of a plant breeding algorithm that would allow to estimate the seed yield at the initial stage of plant growth, based on WUE, SA and H2O2 content.

Biotechnological Potential of LSD1, EDS1, and PAD4 in the Improvement of Crops and Industrial Plants

“…The RCD phenotype is induced by a superoxide anion (O 2 − ) and H 2 O 2 , which are excessively produced in an lsd1 mutant [37,38,39,40,41,42,43,44]. Hormones important for plant defense i.e., salicylic acid (SA) and ethylene (ET) are also over-accumulated in lsd1 [35,40,42,44,45]. It was found that in the NahG/ lsd1 plants that are unable to accumulate SA because of the NahG bacterial gene, encoding salicylate hydroxylase that converts SA to catechol, cell death was suppressed [46].…”

“…LSD1 plays an important role in the response and acclimation of plants to a broad range of stresses such as drought [35,48], UV-C radiation [44,46], cold stress [49], excess light [41], root hypoxia [42] and pathogens [43]. Interestingly, the lsd1 phenotype shows conditional dependence on environmental conditions, and the morphology and seed yield of the mutant does not differ from the wild type when plants are grown under field conditions [35,45]. LSD1 acts as a negative regulator of EDS1 and PAD4 [43,44,45,50,51] in PCD, and double mutants eds1/lsd1 and pad4/lsd1 demonstrate a reverted RCD phenotype, even under stress conditions [44,45].…”

“…Interestingly, the lsd1 phenotype shows conditional dependence on environmental conditions, and the morphology and seed yield of the mutant does not differ from the wild type when plants are grown under field conditions [35,45]. LSD1 acts as a negative regulator of EDS1 and PAD4 [43,44,45,50,51] in PCD, and double mutants eds1/lsd1 and pad4/lsd1 demonstrate a reverted RCD phenotype, even under stress conditions [44,45].…”

“…Mutations in AtEDS1 and AtPAD4 result in impaired SA, ET and ROS homeostasis, disrupted acclimatory responses and cell death signaling [38,42,50,51,54]. However, the role of EDS1 in promoting cell death under biotic and abiotic stresses appears superior to PAD4, and a mutation in AtEDS1 reverses the lsd1 mutant cell death phenotype stronger than the mutation in AtPAD4 [43,45]. It was found that LSD1, EDS1 and PAD4 are involved in lysigenous aerenchyma formation [42].…”

“…LSD1 conformation and its activity are controlled by changes in the PQ pool [64], and it was hypothesized that under stress conditions, changes in the activity of LSD1 can reduce the activity of SOD and CAT proteins, and downregulate PR1 gene expression [51] (Figure 1). Under non-stress laboratory condition, eds1 and pad4 mutants accumulate less H 2 O 2 than wild type plants [45], while double eds1/lsd1 and pad4/lsd1 exhibit similar [35] or lower [41] H 2 O 2 level than wild type.…”