Abstract
Late embryogenesis abundant (LEA) proteins are essential to the ability of resurrection plants and orthodox seeds to protect the subcellular milieu against irreversible damage associated with desiccation. In this work, we investigated the structure and function of six LEA proteins expressed during desiccation in the monocot resurrection species Xerophyta schlechteri (XsLEAs). In silico analyses suggested that XsLEAs are hydrophilic proteins with variable intrinsically disordered protein (IDP) properties. Circular dichroism (CD) analysis indicated that these proteins are mostly unstructured in water but acquire secondary structure in hydrophobic solution, suggesting that structural dynamics may play a role in their function in the subcellular environment. The protective property of XsLEAs was demonstrated by their ability to preserve the activity of the enzyme lactate dehydrogenase (LDH) against desiccation, heat and oxidative stress, as well as growth of Escherichia coli upon exposure to osmotic and salt stress. Subcellular localization analysis indicated that XsLEA recombinant proteins are differentially distributed in the cytoplasm, membranes and nucleus of Nicotiana benthamiana leaves. Interestingly, a LEA_1 family protein (XsLEA1-8), showing the highest disorder-to-order propensity and protective ability in vitro and in vivo, was also able to enhance salt and drought stress tolerance in Arabidopsis thaliana. Together, our results suggest that the structural plasticity of XsLEAs is essential for their protective activity to avoid damage of various subcellular components caused by water deficit stress. XsLEA1-8 constitutes a potential model protein for engineering structural stability in vitro and improvement of water-deficit stress tolerance in plants.
Highlights
Water availability is one of the major environmental factors that affect plant growth, development and productivity
The expression of the six XsLEAs used in our analysis has been reported by Costa et al (2017) to be increased in X. schlechteri leaves upon desiccation between 60% RWC (1.5 gH2O g−1 dwt) and 40% RWC (1.0 gH2O g−1 dwt) (Supplementary Figure 1), coinciding with the activation of the molecular signature of the resurrection physiology
These results suggest that the transgenic lines expressing XsLEA1-8 may display a better control of water loss during drying, which may enhance their survival (Supplementary Figure 9C). These findings point toward a potential role of XsLEA1-8 in enhancing osmotic stress tolerance in plants. Since their discovery as accumulating during the later stages of seed embryogenesis, increasing evidence suggests a protective function of Late embryogenesis abundant (LEA) proteins against desiccation and other stresses, leading to great interest in the structural dynamics of these proteins in the subcellular environment
Summary
Water availability is one of the major environmental factors that affect plant growth, development and productivity. During their life cycle, plants may endure periods of environmental drought and, depending on the duration of such periods, it may lead to irreversible structural damages affecting plant development and survival. A group of about 135 angiosperm plant species have been described as “resurrection plants” for their ability to tolerate the loss of 80% to 95% of cellular water and resume photosynthetic activity and growth within hours after rehydration (Oliver et al, 2000; Scott, 2000; Porembski, 2011; Farrant et al, 2015). X. schlechteri is a resurrection monocot species, phylogenetically related to most important grass crops from the Poaceae family, and understanding its DT opens opportunities to apply this knowledge to improve drought tolerance in crops (Farrant et al, 2015; Costa et al, 2017)
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