Balancing growth amidst salinity stress – lifestyle perspectives from the extremophyte model Schrenkiella parvula

Abstract

The use of extremophyte models to select growth promoting traits during environmental stresses is a recognized yet an underutilized strategy to design stress-resilient plants. Schrenkiella parvula, a leading extremophyte model in Brassicaceae, can grow and complete its life cycle under multiple environmental stresses, including high salinity. While S. parvula is equipped with foundational genomic resources to identify genetic clues that potentially lead to stress adaptations at the phenome level, a comprehensive physiological and structural characterization of salt stress responses throughout its lifecycle is absent. We aimed to identify the influential traits that lead to resilient growth and strategic decisions to ensure survival of the species in an extreme environment, and examined salt-induced changes in the physiology and anatomy of S. parvula throughout its life cycle across multiple tissues. We found that S. parvula maintains or even enhances growth during various developmental stages at salt stress levels known to inhibit growth in Arabidopsis thaliana and most crops. The resilient growth of S. parvula was associated with key traits synergistically allowing continued primary root growth, expansion of xylem vessel elements across the root-shoot continuum, and the high capacity to maintain tissue water levels by developing larger and thicker leaves while facilitating continued photosynthesis during salt stress. In turn, the stress-resilient growth during the vegetative phase of S. parvula allowed a successful transition to a reproductive phase via early flowering followed by the development of larger siliques with viable seeds on salt-treated plants. Additionally, the success of self-fertilization in early flowering stages was dependent on salt-induced filament elongation. Our results suggest that the maintenance of leaf water status and enhancement of selfing in early flowers to ensure reproductive success are among the most influential traits that contribute to the extremophilic lifestyle of S. parvula in its natural habitat.

Multiple paths lead to salt tolerance - pre-adaptation vs dynamic responses from two closely related extremophytes

“…Some of these metabolites that are high at basal levels may have added benefits for serving as osmoprotectants or antioxidants when a slow-growing annual such as E. salsugineum experiences high salinity levels. Schrenkiella parvula dynamically accumulates these metabolites during salt treatments, without an indication of compromised growth, to match the levels maintained in E. salsugineum (Figures 4 and 5) 58 .…”

“…Schrenkiella parvula dynamically accumulates these metabolites during salt treatments, without an indication of compromised growth, to match the levels maintained in E. salsugineum (Figures 4 and 5) 58 .…”

Effective root responses to salinity stress include maintained cell expansion and carbon allocation

“…It has been reported that a middle cortex (MC) initiates from endodermal cells of Arabidopsis roots 7 days after germination (Cui, 2016). We previously showed the extra layer in roots of S. parvula initiates from the endodermis (Tran et al , 2021a), implying it could be MC. To further understand the initiation of this cell layer, we analyzed the presence of MC in different developmental stages of S. parvula and Arabidopsis seedlings.…”

“…The copyright holder for this this version posted September 1, 2022. ; https://doi.org/10.1101/2022.09.01.506200 doi: bioRxiv preprint Arabidopsis (Tran et al, 2021a). We further compared relative changes of suberization under salt stress and found the fully-suberized zone in S. parvula increased around 3 times in length under 125mM NaCl, and even further under 175mM NaCl, whereas it increased less than 2 times under 125mM NaCl and did not increase under 175mM NaCl in Arabidopsis (Fig.…”

“…Furthermore, lateral root elongation is reduced more than that of the primary root (Julkowska et al , 2014). S. parvula seedlings experienced much less inhibition of primary root growth by salt compared to Arabidopsis, and were also insensitive to treatment with the stress hormone, abscisic acid (ABA) (Tran et al , 2021a; Sun et al , 2022). At the cellular level, salt suppresses root growth by interfering with cell cycle progression in the root apical meristem (RAM) and by reducing elongation of mature cells (West et al , 2004).…”