Differential Response to Single and Combined Salt and Heat Stresses: Impact on Accumulation of Proteins and Metabolites in Dead Pericarps of Brassica juncea

Abstract

Dead organs enclosing embryos, such as seed coats and pericarps, are emerging as important maternally-derived components of the dispersal unit that affect seed performance and fate. In the face of climate change and increased incidents of heatwaves, we sought to investigate the effect of salinity (S), short episodes of high temperature (HS), and combination of S + HS (SHS), at the reproductive phase, on the properties of dead pericarps of Brassica juncea. Proteome and metabolome analyses revealed multiple proteins and metabolites stored in dead pericarps whose levels and composition were altered under single and combined stress conditions. The protein profile of SHS showed a higher correlation with salt than with HS indicating the dominant effect of salt over heat stress. On the other hand, the analysis of metabolites showed that the profile of SHS has better correlation with HS than with salt. The integration of metabolic and proteomic data showed that changes in TCA cycle intermediates and certain amino acids (e.g., proline) under salt treatments (S and SHS) are highly correlated with changes in proteins involved in their biosynthetic pathways. Thus, accumulation of proteins and metabolites in dead pericarps is differently affected by single and combination of salt and heat stresses. Salinity appears to dominate plant response to combined stresses at the protein level, while heat appears to be the major factor affecting metabolite accumulation in dead pericarps.

Single and Combined Salinity and Heat Stresses Impact Yield and Dead Pericarp Priming Activity

“…Since the realization that plants respond uniquely to a combination of stresses [ 14 ], which is not merely the summation responses to each stress, multiple reports have been published addressing plant response to single and combined stresses. Accordingly, these reports clearly approved the idea that a combination of stresses often yields a specific response, which is not seen under either single stress condition [ 15 , 16 , 17 , 18 ]. Yet, a combination of stresses not only elicits a specific response but may either mitigate [ 19 ] or enhance [ 20 , 21 ] the stress effect.…”

“…While most studies addressing plant response to single or combined stresses focused on crop yield or on vegetative growth performance, not many studies have addressed the effect on the maternally-derived dead components of the dispersal unit (e.g., seed coat, pericarps), designated dead organs enclosing embryos (DOEEs). Recent work demonstrated that the maternal environment not only affects the embryo properties but also the properties of DOEEs [ 18 , 22 , 23 ]. Besides providing a shield for embryo protection and a means for dispersal, DOEEs also function as a long-term storage for multiple substances (proteins, metabolites) that can persist in active form for decades and affect seed germination and fate [ 24 , 25 , 26 ].…”

“…Besides providing a shield for embryo protection and a means for dispersal, DOEEs also function as a long-term storage for multiple substances (proteins, metabolites) that can persist in active form for decades and affect seed germination and fate [ 24 , 25 , 26 ]. The expected changes in the DOEEs properties as a result of the maternal environment [ 18 , 22 , 23 ] can have an impact on seed viability and persistence, germination and seedling establishment and consequently on plant population dynamics and diversity [ 27 , 28 , 29 , 30 ].…”

What Worth the Garlic Peel

“…In recent years, several reports have uncovered the elaborated function of DOEEs acting as long-term storage for active proteins, including hydrolases (e.g., nucleases, chitinases, and proteases), reactive oxygen species (ROS) detoxifying enzymes, and cell wall-modifying enzymes. In addition, DOEEs store and release numerous substances upon hydration, such as phytohormones, sugars, amino acids, and substances that control microbial growth and germination of heterologous species [5][6][7][8][9][10]. Many heat shock proteins (HSPs) (e.g., HSP90, HSP70, sHSPs), which are often induced in response to multiple stresses [11,12], are also accumulated in DOEEs [8,10,13].…”

“…In addition, DOEEs store and release numerous substances upon hydration, such as phytohormones, sugars, amino acids, and substances that control microbial growth and germination of heterologous species [5][6][7][8][9][10]. Many heat shock proteins (HSPs) (e.g., HSP90, HSP70, sHSPs), which are often induced in response to multiple stresses [11,12], are also accumulated in DOEEs [8,10,13]. Numerous reports highlighted the positive effect of DOEEs on seed longevity, seed germination, and seedling performance [5,[13][14][15][16][17].…”