Variations of Secondary Metabolites among Natural Populations of Sub-Antarctic Ranunculus Species Suggest Functional Redundancy and Versatility

Abstract

Plants produce a high diversity of metabolites which help them sustain environmental stresses and are involved in local adaptation. However, shaped by both the genome and the environment, the patterns of variation of the metabolome in nature are difficult to decipher. Few studies have explored the relative parts of geographical region versus environment or phenotype in metabolomic variability within species and none have discussed a possible effect of the region on the correlations between metabolites and environments or phenotypes. In three sub-Antarctic Ranunculus species, we examined the role of region in metabolite differences and in the relationship between individual compounds and environmental conditions or phenotypic traits. Populations of three Ranunculus species were sampled across similar environmental gradients in two distinct geographical regions in îles Kerguelen. Two metabolite classes were studied, amines (quantified by high-performance liquid chromatography and fluorescence spectrophotometry) and flavonols (quantified by ultra-high-performance liquid chromatography with triple quadrupole mass spectrometry). Depending on regions, the same environment or the same trait may be related to different metabolites, suggesting metabolite redundancy within species. In several cases, a given metabolite showed different or even opposite relations with the same environmental condition or the same trait across the two regions, suggesting metabolite versatility within species. Our results suggest that metabolites may be functionally redundant and versatile within species, both in their response to environments and in their relation with the phenotype. These findings open new perspectives for understanding evolutionary responses of plants to environmental changes.

A New Catalog of Structural Variants in 1,301 A. thaliana Lines from Africa, Eurasia, and North America Reveals a Signature of Balancing Selection at Defense Response Genes

“…2013 ). Further, plants produce a massive number of metabolites and only a few of these are primary (those common to all organisms); others are known as secondary metabolites ( Pichersky and Gang 2000 ; Labarrere et al. 2019 ).…”

Low‐temperature tolerance of the Antarctic species Deschampsia antarctica: A complex metabolic response associated with nutrient remobilization

“…Several studies have reported significant changes in carbon and nitrogen metabolism in response to cold conditions, including, but not limited to: (a) accumulation of sucrose and fructose, which could act as cryoprotectants (Cook et al, ); (b) synthesis of fructans and raffinose, which could play a role as membrane stabilizers and antioxidants (Klotke, Kopka, Gatzke, & Heyer, ; Van den Ende, ); (c) general accumulation of amino acids, such as asparagine, aspartate, glutamine, and glutamate (Bocian et al, ; Klotke et al, ); (d) shifts in the plastidial pools of asparagine, glutamine, and glutamate through an aspartate shuttle, to remove the excess of redox equivalents to the mitochondria (Hoermiller et al, ); (e) impaired nitrogen assimilation by reducing the activity of key enzymes, such as nitrate/nitrite reductases and glutamine/glutamate synthetases (Goel & Singh, ), and (f) sulfur metabolism linked to polyamine synthesis and secondary metabolism (Clemente‐Moreno, Omranian, et al, ; Labarrere, Prinzing, Dorey, Chesneau, & Hennion, , and references therein).…”

Phytochemical Variation within Aerial Parts of Ferula cupularis Populations, an Endangered Medicinal Plant from Iran

“…Wild populations are formed by closely related plants in nature, and plants from various populations generally exhibit greater evolutionary variations compared to ones belong to the same population. [1] The majority of Central Asia. [4,5] This genus represented 32 species in Iran, 15 of which are endemic.…”

“…Despite the fact that secondary metabolites play an important role in the plants’ adaptability, natural phytochemical variations and subsequently different bioactivities are inevitable to occur among different populations located in various regions. Wild populations are formed by closely related plants in nature, and plants from various populations generally exhibit greater evolutionary variations compared to ones belong to the same population [1] . The majority of Iranian native medicinal plants have a wide geographical distribution and grow spontaneously in a range of bioclimatic zones [2] .…”