Evolutionary Divergences in Root Exudate Composition among Ecologically-Contrasting Helianthus Species

Abstract

Plant roots exude numerous metabolites into the soil that influence nutrient availability. Although root exudate composition is hypothesized to be under selection in low fertility soils, few studies have tested this hypothesis in a phylogenetic framework. In this study, we examined root exudates of three pairs of Helianthus species chosen as phylogenetically-independent contrasts with respect to native soil nutrient availability. Under controlled environmental conditions, seedlings were grown to the three-leaf-pair stage, then transferred to either high or low nutrient treatments. After five days of nutrient treatments, we used gas chromatography-mass spectrometry for analysis of root exudates, and detected 37 metabolites across species. When compared in the high nutrient treatment, species native to low nutrient soils exhibited overall higher exudation than their sister species native to high nutrient soils in all three species pairs, providing support for repeated evolutionary shifts in response to native soil fertility. Species native to low nutrient soils and those native to high nutrient soils responded similarly to low nutrient treatments with increased exudation of organic acids (fumaric, citric, malic acids) and glucose, potentially as a mechanism to enhance nutrition acquisition. However, species native to low nutrient soils also responded to low nutrient treatments with a larger decrease in exudation of amino acids than species native to high nutrient soils in all three species pairs. This indicates that species native to low nutrient soils have evolved a unique sensitivity to changes in nutrient availability for some, but not all, root exudates. Overall, these repeated evolutionary divergences between species native to low nutrient soils and those native to high nutrient soils provide evidence for the adaptive value of root exudation, and its plasticity, in contrasting soil environments.

Metabolite profiling of non‐sterile rhizosphere soil

“…Although it is known that microbial diversity in the rhizosphere can influence plant growth and health (Berendsen et al, 2012), the chemical signals mediating these interactions remain poorly understood. The majority of root exudation studies are based on hydroponic and/or sterile growth systems (Khorassani et al, 2011;Kuijken et al, 2014;Bowsher et al, 2016). Although sterile growth systems are appropriate for the exact quantification of root-exuded plant chemicals (Kuijken et al, 2014), these systems do not consider the importance of rhizosphere signals that are of microbial origin, such as microbial breakdown products of root exudates, or metabolites that are specifically produced by rhizosphere-inhabiting microbes.…”

“…The environmental effects of root exudation chemistry have been studied mostly in (semi)sterile hydroponic systems (Song et al, 2012;Vranova et al, 2013;da Silva Lima et al, 2014). An important justification for the use of such soil-free growth conditions is that they allow for the tight maintenance of environmental variables (Ziegler et al, 2015;Bowsher et al, 2016). In addition, hydroponic growth systems prevent sorption of metabolites to soil particles and microbial degradation.…”

Rhizophagy Cycle: An Oxidative Process in Plants for Nutrient Extraction from Symbiotic Microbes

“…Plants produce a root exudate zone adjacent to and just behind root tip meristems [ 58 ]. Plants secrete carbohydrates, amino acids, vitamins and organic acids into this zone [ 59 ]. The literature suggests that plants alter numbers and diversity of microbes on root surfaces and in the rhizosphere through secretion of exudates [ 60 ].…”

“…The literature suggests that plants alter numbers and diversity of microbes on root surfaces and in the rhizosphere through secretion of exudates [ 60 ]. Plants are known to increase secretion of exudates in nutrient limiting soils, likely leading to increased microbial activity around roots and increased ‘microbial mining’ for nutrients [ 59 ]. Root exudates attract microbes that will grow in the root exudates [ 58 , 61 ].…”

Fertilizer and intercropped legumes as nitrogen source for Jerusalem artichoke (Helianthus tuberosus L.) tops for bioenergy

“…Jerusalem artichoke has shown a strong ability to extract nutrients from soils (Cors and Falisse 1980) and it may be that its root exudates are effective at promoting the breakdown of soil organic matter, freeing mineral N that is then taken up. The literature on root exudates from Helianthus species is surprisingly scarce (Bowsher et al 2016). Soil organic N concentrations are high on the Viikki farm, following five centuries of cattle farming (Tammeorg et al 2014).…”