Environmental Signals Act as a Driving Force for Metabolic and Defense Responses in the Antarctic Plant Colobanthus quitensis
During evolution, plants have faced countless stresses of both biotic and abiotic nature developing very effective mechanisms able to perceive and counteract adverse signals. The biggest challenge is the ability to fine-tune the trade-off between plant growth and stress resistance. The Antarctic plant Colobanthus quitensis has managed to survive the adverse environmental conditions of the white continent and can be considered a wonderful example of adaptation to prohibitive conditions for millions of other plant species. Due to the progressive environmental change that the Antarctic Peninsula has undergone over time, a more comprehensive overview of the metabolic features of C. quitensis becomes particularly interesting to assess its ability to respond to environmental stresses. To this end, a differential proteomic approach was used to study the response of C. quitensis to different environmental cues. Many differentially expressed proteins were identified highlighting the rewiring of metabolic pathways as well as defense responses. Finally, a different modulation of oxidative stress response between different environmental sites was observed. The data collected in this paper add knowledge on the impact of environmental stimuli on plant metabolism and stress response by providing useful information on the trade-off between plant growth and defense mechanisms.
Keywords: Colobanthus quitensis; differential proteomic analysis; environmental signals; enzymatic activity; gene expression analysis; MS/MS analysis; response to stress
Antarctica was the last continent to be discovered, likely due to its harsh environment and geographical isolation from other regions of the Earth. Climatic and environmental conditions are so severe that they do not allow the development of numerous species as in other regions of our planet. Indeed, this holds true especially for vascular plants that grow only in the Antarctic Peninsula, which is characterized by milder conditions. In fact, its temperatures are warmer, exceeding 0 °C during the Antarctic summer and rarely dropping below −10 °C during the Antarctic winter . Nonetheless, sub-zero temperatures are also characteristic of the austral summer during the night, particularly on King George Island (South Shetland) [2,3]. Although these conditions are milder than those of the Antarctic continent, Maritime Antarctica still represents an extreme ecosystem where the inhabiting organisms experience low temperatures, restricted availability of water and nutrients, high radiation, and wind abrasion [4,5,6,7].
The Antarctic Peninsula hosts two species of endemic flowering plants: the Antarctic hairgrass Deschampsia antarctica E. Desv. (Poaceae) and the Antarctic pearlwort Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) . Furthermore, two more species were introduced accidentally in this region, both belonging to the Poaceae family, i.e., Poa pratensis L. and Poa annua L. [9,10]. In addition, one more non-native plant belonging to the Juncaceae family has been identified in association with the endemic Antarctic plants, i.e., Juncus bufonius L. . Apart from the newly introduced species, only D. antarctica and C. quitensis have been able to naturally colonize a vast part of Maritime Antarctica down to ca. 68° S, spreading to the west coast of the Antarctic Peninsula and its associated islands . Indeed, C. quitensis has a wider area of colonization, also extending along the Andes to Ecuador, with a site in Mexico .
These plant species have developed a moderate to perfect adaptation to cold and frost and have also been experiencing the effect of rising temperatures over the last decades. Both species are able to acclimate to the cold by modulating their LT50 (lethal temperature at 50%), i.e., the temperature at which 50% of the leaf tissue dies due to freezing, and are therefore considered freezing-tolerant species [2,14]. Along with the mechanisms of freezing resistance, other biochemical, physiological, and morphological adaptations occurred during evolution, allowing their survival and spread in the harsh Antarctic environment. Anatomical and ultrastructural modifications have been reported for D. antarctica which has several xerophytic characteristics, such as small and thick leaves, high stomata density per area, thick cuticle, and high morphological plasticity of organs and organelles . C. quitensis has linear and sessile leaves also showing typically xeric characteristics, such as high thickness, higher density of diacytic stomata found on both leaf surfaces (amphistomatic leaf), and the presence of the bundle sheath that minimizes apoplastic water movement toward mesophyll particularly dense and poor in cell wall fibers . Furthermore, C. quitensis has a cushion conformation called pearlwort that allows reduced exposure to abiotic stresses such as strong winds and poor water availability compared to D. antarctica. In addition, both plants developed many physiological adaptations such as the ability to maintain a positive photosynthetic rate near 0 °C, resistance to photoinhibitory conditions, and tolerance to water stress . Furthermore, it has also been demonstrated that C. quitensis populations show anatomical and physiological adaptation along a latitudinal gradient, and individuals inhabiting cold zones at high latitudes increase their ecophysiological performance under simulated global warming conditions more than northernmost populations . These plants have been recognized over the past years as bioindicators of climate change. Indeed, it has been hypothesized that their expansion and diffusion could be mainly triggered by summer air warming [17,18]. Beyond temperature change, extremophilic plants also have to cope with other harsh environmental conditions that can act as a trigger for the activation of defense mechanisms against (a)biotic stress or adaptation strategies. Among the latter, the role of endophytic microorganisms is emerging as one of the many strategies to deal with extreme environmental conditions, although the peculiar traits are starting to be deepened [19,20,21].
In recent years, we performed the de novo transcriptome assembly of C. quitensis plants grown in a low-temperature natural habitat compared to plants grown for one year inside open-top chambers (OTCs), which determine an increase of about 4 °C at midday . In addition, we shed some light on the proteome remodeling of C. quitensis grown under the same experimental conditions using a differential proteomic approach . Overall, these results reveal that C. quitensis plants grown at warmer temperatures display a high rate of photorespiration which likely acts as a protective mechanism against photooxidative damage, ROS production, and lipid peroxidation . These results are in agreement with those reported by Cho et al.  who compared the transcriptome of C. quitensis plants grown in the natural cold habitat versus those grown under milder growth conditions in the laboratory.
Due to the progressive environmental change to which the Antarctic Peninsula is subjected over time, a more comprehensive overview of the metabolic characteristics of local plants becomes particularly interesting for evaluating their ability to deal with environmental stresses. This work aimed to investigate the C. quitensis proteome rewiring triggered by environmental cues by using an integrated differential proteomic approach. To this end, plants from three different sites were analyzed. The sites differ in several environmental conditions near the Antarctic Polish base Henrik Arctowski (King George Island, South Shetland). Among them are the distance from the coastline, altitude, air temperature, wind speed, and soil composition. The data collected in this work, combined with the information available in the literature, add knowledge on the impact of environmental stimuli on plant metabolism and stress response by providing useful information on the trade-off between plant growth and defense mechanisms.
In Press – Climate Change
Laura Bertini, Silvia Proietti, Benedetta Fongaro, Aleš Holfeld, Paola Picotti, Gaia Salvatore Falconieri, Elisabetta Bizzarri, Gloria Capaldi, Patrizia Polverino de Laureto,Carla Caruso
21 November 2022
Multidisciplinary Digital Publishing Institute / www.mdpi.com