Another Tale from the Harsh World: How Plants Adapt to Extreme Environments

Abstract

The environmental fluctuations of a constantly evolving world can mould a changing context, often unfavourable to sessile organisms that must adjust their resource allocation between both resistance or tolerance mechanisms and growth. Plants bear the fascinating ability to survive and thrive under extreme conditions, a capacity that has always attracted the curiosity of humans, who have discovered and improved species capable of meeting our physiological needs. In this context, plant research has produced a great wealth of knowledge on the responses of plants to a range of abiotic stresses, mostly considering model species and/or controlled conditions. However, there is still minimal comprehension of plant adaptations and acclimations to extreme environments, which cries out for future investigations. In this article, we examined the main advances in understanding the adapted traits fixed through evolution that allowed for plant resistance against abiotic stress in extreme natural ecosystems. Spatio‐temporal adaptations from extremophile plant species are described from morpho‐anatomical features to physiological function and metabolic pathways adjustments. Considering that metabolism is at the heart of plant adaptations, a focus is given to the study of primary and secondary metabolic adjustments as well as redox metabolism under extreme conditions. This article further casts a critical glance at the main successes in studying extreme environments and examines some of the challenges and opportunities this research offers, especially considering the possible interaction with ecology and metaphenomics.

Predictive metabolomics of multiple Atacama plant species unveils a core set of generic metabolites for extreme climate resilience

“…Conversely, raffinose negatively correlated with temperature, validating the central place of raffinose family oligosaccharides in cold tolerance (Vinson et al ., 2020). However, several predictors were fatty acyls within the primary metabolism and jasmonates, which supported a role of lipid remodelling in extreme environments (Cao et al ., 2016; Dussarrat et al ., 2021).…”

“…Remarkably, phenolics (14/39 compounds) were increased at lower elevations, which would help plants cope with both the very low water availability and high salinity of these lands. This protective process has already been described in multiple extremophile plant species (Dussarrat et al ., 2021). Phenolic antioxidant properties, mainly for cinnamic acid and quercetin derivatives (extensively represented in the best predictors), enhance photoprotection and resilience to abiotic stresses (Agati & Tattini, 2010).…”

“…In this scenario, returning to wild plant species that live and thrive in some of the harshest environments on Earth offers an opportunity to find new strategies for crop improvement (Castañeda‐Álvarez et al ., 2016). Recent studies have pinpointed relevant metabolic clusters in adaptation to extreme environments in plants harvested in high mountains, deserts and salt lands (Dussarrat et al ., 2021). These adaptive mechanisms involved the accumulation of amino acids (Lugan et al ., 2010) as precursors of secondary metabolites, and carotenoids (Cui et al ., 2019) and polyphenols (Hashim et al ., 2020) as processors of reactive oxygen species (ROS).…”

“…These adaptive mechanisms involved the accumulation of amino acids (Lugan et al ., 2010) as precursors of secondary metabolites, and carotenoids (Cui et al ., 2019) and polyphenols (Hashim et al ., 2020) as processors of reactive oxygen species (ROS). In addition, most of these studies were carried out on a unique or limited number of species (Dussarrat et al ., 2021), which, combined with high biochemical diversity, led to highly specific metabolic markers involved in adaptive mechanisms exclusive to the species or environment (Peters et al ., 2018; Dussarrat et al ., 2021).…”

Transcriptomic analysis of the C3-CAM transition in Cistanthe longiscapa, a drought tolerant plant in the Atacama Desert

“…In the upcoming years, it is expected that temperatures and drought periods will intensify due to climate change, affecting biodiversity at all levels (Feng and Fu, 2013; Schlaepfer et al ., 2017), with terrestrial plants particularly exposed to these stressful environmental factors (Feng and Fu, 2013; Parmesan and Hanley, 2015; Schlaepfer et al ., 2017). Plants can sense environmental changes rapidly and evolve morphological, physiological, and molecular adaptations to face them (Dussarrat et al ., 2018). However, the mechanisms underlying these responses are still unknown, making it difficult to build any prediction model on how plants will face the aforementioned challenges.…”