The Fermentation Analogy: A Point of View for Understanding the Intriguing Role of Proline Accumulation in Stressed Plants

The accumulation of proline under environmental stress is a conserved response of plants. Five decades have passed since the first report of proline accumulation in plants (Barnnet and Naylor, 1966). Many hypotheses have been put forward regarding assignment of a function to proline. These proposed roles include antioxidant capacity, osmoprotection, signaling, developmental function, and contributing in redox and cellular homeostasis Among these, the osmotic adjustment, osmoprotectant, and antioxidant role have probably been the earliest and most widely accepted functions of proline. It is known that compatible osmolytes contribute in the retention of water, but also some of them force proteins to adopt a compactly folded structure, preventing the unfolding and reducing the exposed surface of the protein to damaging compounds (Attri et al., 2010). In case of proline this was demonstrated both in vitro and in single cell organisms. For example, it was observed that proline overproducing E. coli mutants had greater osmotolerance (Csonka et al., 1988) and also proline can inhibit protein aggregation in vivo (Ignatova and Gierasch, 2006). However, neither osmotic adjustment nor osmoprotection has been clearly confirmed in plants (Maggio et al., 2002; Kavi Kishor and Sreenivasulu, 2014). This is probably more complex in plants because plants have different osmoregulatory mechanisms. Controversy is present regarding its proposed antioxidant role because recent evidence demonstrates that proline cannot scavenge singlet oxygen, superoxide, nitric oxide, peroxynitrite nor nitrogen dioxide (Signorelli et al., 2013, 2016). In view of the lack of activity in previously suggested roles it has recently been proposed that proline acts exclusively as a hydroxyl radical scavenger (Signorelli et al., 2014, 2015), but more evidence for the physiological importance of this role is needed. Recently, the availability of proline biosynthesis Arabidopsis knockout (KO) mutant plants has allowed researchers to provide direct evidence regarding the role of proline in plants. It was observed that one of these mutants (p5cs2 mutant) were embryo lethal (Szekely et al., 2008) and that proline is required for flower transition and for pollen development and transmission (Mattioli et al., 2009, 2012; Funck et al., 2012). Additionally, it has been shown that proline content in roots correlates with root development (Sharma et al., 2011; Biancucci et al., 2015). This evidence clearly demonstrates the involvement of proline in development. However, the purpose of the accumulation of large amounts of proline in leaves under stressful conditions remains unresolved.