Mitochondrial Small Heat Shock Proteins Are Essential for Normal Growth of Arabidopsis thaliana.

Mariela R Escobar,Estela M Valle,Ivo Feussner

doi:10.3389/fpls.2021.600426

Abstract

Mitochondria play important roles in the plant stress responses and the detoxification of the reactive oxygen species generated in the electron transport chain. Expression of genes encoding stress-related proteins such as the mitochondrial small heat shock proteins (M-sHSP) is upregulated in response to different abiotic stresses. In Arabidopsis thaliana, three M-sHSPs paralogous genes were identified, although their function under physiological conditions remains elusive. The aim of this work is to uncover the in vivo function of all three M-sHSPs at the whole plant level. To accomplish this goal, we analyzed the phenotype, proteomic, and metabolic profiles of Arabidopsis knock-down lines of M-sHSPs (single, double, and triple knock-down lines) during normal plant growth. The triple knock-down plants showed the most prominent altered phenotype at vegetative and reproductive stages without any externally applied stress. They displayed chlorotic leaves, growth arrest, and low seed production. Concomitantly, they exhibited increased levels of sugars, proline, and citric, malic, and ascorbic acid, among other metabolites. In contrast, single and double knock-down plants displayed a few changes in their phenotype. A redundant function among the three M-sHSPs is indicated by the impairment in vegetative and reproductive growth associated with the simultaneous loss of all three M-sHSPs genes. The triple knock-down lines showed alteration of proteins mainly involved in photosynthesis and antioxidant defense compared to the control plants. On the other hand, heat stress triggered a distinct cytosolic response pattern and the upregulation of other sHSP members, in the knock-down plants. Overall, depletion of all three M-sHSPs in Arabidopsis severely impacted fundamental metabolic processes, leading to alterations in the correct plant growth and development. These findings expand our knowledge about the contribution of organelle-specific M-sHSPs to healthy plant growth under non-stress conditions.

Highlights

In plants, reactions involved in regular metabolisms, such as photosynthesis and respiration, are sources of reactive oxygen species (ROS) in the cell as the unavoidable consequence of aerobic life (Halliwell and Gutteridge, 2015)
M-sHSP23.5 and M-sHSP23.6 promoters were active in all tissues after heat treatment, while M-sHSP26.5 promoter activity was only detectable in the root
We present evidence that the simultaneous downregulation of all three Arabidopsis mitochondrial small heat shock proteins (M-sHSP) is essential for plant growth and development under normal growing conditions

Summary

Introduction

Reactions involved in regular metabolisms, such as photosynthesis and respiration, are sources of reactive oxygen species (ROS) in the cell as the unavoidable consequence of aerobic life (Halliwell and Gutteridge, 2015). Mitochondria generate much more ROS than other cell compartments (Zhang et al, 2009). Plant sHSPs respond to a wide range of environmental stresses (Wang et al, 2004; Jacob et al, 2017), and sHSP gene expression is mediated by the increase in cellular H2O2 accumulation in Arabidopsis thaliana (Vanderauwera et al, 2005; Scarpeci et al, 2008a). SHSP genes are hardly expressed in vegetative tissue under non-stress conditions (Waters et al, 1996; Scarpeci et al, 2008b). The protective function of sHSPs in stress responses is quite conserved among different plant species. Overexpression of tea (Camellia sinensis) sHSP genes confers tolerance to heat and cold stress in Arabidopsis (Wang et al, 2017). SHSP21 is responsible for the development of chloroplasts during heat stress (Zhong et al, 2013)

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