Functional roles of microbial symbionts in plant cold tolerance

Abstract

In this review, we examine the functional roles of microbial symbionts in plant tolerance to cold and freezing stresses. The impacts of symbionts on antioxidant activity, hormonal signaling and host osmotic balance are described, including the effects of the bacterial endosymbionts Burkholderia, Pseudomonas and Azospirillum on photosynthesis and the accumulation of carbohydrates such as trehalose and raffinose that improve cell osmotic regulation and plasma membrane integrity. The influence of root fungal endophytes and arbuscular mycorrhizal fungi on plant physiology at low temperatures, for example their effects on nutrient acquisition and the accumulation of indole-3-acetic acid and antioxidants in tissues, are also reviewed. Meta-analyses are presented showing that aspects of plant performance (shoot biomass, relative water content, sugar and proline concentrations and F v /F m ) are enhanced in symbiotic plants at low (À1 to 15°C), but not at high (20-26°C), temperatures. We discuss the implications of microbial symbionts for plant performance at low and sub-zero temperatures in the natural environment and propose future directions for research into the effects of symbionts on the cold and freezing tolerances of plants, concluding that further studies should routinely incorporate symbiotic microbes in their experimental designs.

Brassica oleracea var. acephala (kale) improvement by biological activity of root endophytic fungi

“…In this sense, several authors have described different mechanisms such as heat shock proteins or antioxidant compounds that, for example, the endophyte C. globosum has to tolerate cold, some of which may also be beneficial for the plant thanks to the interaction [45][46][47] . The interaction of B. oleracea with Phialocephala also produced an increase in plant tolerance to cold, as has been verified in different subarctic herbaceous plants by Phialocephala fortinii 48 . Also, we have observed the capacity of Diaporthe sp.…”

Fungal Symbionts Enhance N-Uptake for Antarctic Plants Even in Non-N Limited Soils

“…In cold environments as polar and alpine regions the edaphic nitrogen is mainly available as organic compound, imposing metabolic restrictions to the biological mineralization of nitrogen (Shaver and Chapin, 1980;Pietr et al, 1983;Atkin, 1996). To cope with the inorganic N scarcity, plants take advantage of symbiotic interaction with microorganisms (e.g., root mycorrhizal symbionts and root endophytes), as a strategy to enhance their nutritional status (Hobbie et al, 2000;Newsham, 2011;Acuña-Rodríguez et al, 2020). The benefit of the interactions, as described in plant-mycorrhyzae interactions from the Arctic tundra (Hobbie and Högberg, 2012), are related to the capacity of the microbial symbionts to mineralize complex organic N compounds into inorganic forms like ammonium (NH 4 + ) and nitrate (NO 3 − ), which are easily absorbed by the plant's roots.…”

“…When supplied with inorganic N, some detrimental effects on the plant were observed (Upson et al, 2009a), presumably because both plant and fungi compete for soil resources, shifting the plant-DSE association from beneficial to negative for the host. Thus, the positive role of DSE root-symbionts on their host plants' performance is still not conclusive and appears to be highly dependent on the environmental conditions (Newsham, 2011;Acuña-Rodríguez et al, 2020).…”

“…Nevertheless, unlike most plant communities, the microbiota associated to the roots of the Antarctic plants is dominated by DSE instead of mycorrhizal fungi (Upson et al, 2009b). Antarctic endophytes and mycorrhizal fungi, however, seem to play a similar ecological role enhancing nutrient acquisition and N in particular (Hill et al, 2019;Acuña-Rodríguez et al, 2020).…”

Maternal Exposure to Ozone Modulates the Endophyte-Conferred Resistance to Aphids in Lolium multiflorum Plants

“…In addition to the alkaloid-mediated herbivore resistance, endophytes can be source of other metabolites with functional roles such as phenolic compounds [ 35 , 36 , 37 ]), antioxidants [ 38 , 39 , 40 ] and phytohormones [ 41 ]. These are suggested to explain the usually documented higher performance of endophyte-symbiotic plants, relative to endophyte-free plants, under conditions of stress caused by biotic (competing plants, herbivores, pathogens) and abiotic factors (drought, heavy metal, herbicides) [ 38 , 39 , 40 , 42 , 43 , 44 , 45 ]. Nonetheless, the endophyte effects on host plant performance have been shown to depend on the ecological context and thus, symbiosis outcome can yield positive, neutral, or even negative [ 46 , 47 , 48 ].…”