Legumes Modulate Allocation to Rhizobial Nitrogen Fixation in Response to Factorial Light and Nitrogen Manipulation

Abstract

The costs and benefits that define gain from trade in resource mutualisms depend on resource availability. Optimal partitioning theory predicts that allocation to direct uptake versus trade will be determined by both the relative benefit of the resource acquired through trade and the relative cost of the resource being traded away. While the costs and benefits of carbon:nitrogen exchange in the legume–rhizobia symbiosis have been examined in depth with regards to mineral nitrogen availability, the effects of varying carbon costs are rarely considered. Using a growth chamber experiment, we measured plant growth and symbiosis investment in the model legume Medicago truncatula and its symbiont Ensifer medicae across varying nitrogen and light environments. We demonstrate that plants modulate their allocation to roots and nodules as their return on investment varies according to external nitrogen and carbon availabilities. We find empirical evidence that plant allocation to nodules responds to carbon availability, but that this depends upon the nitrogen environment. In particular, at low nitrogen—where rhizobia provided the majority of nitrogen for plant growth—relative nodule allocation increased when carbon limitation was alleviated with high light levels. Legumes’ context-dependent modulation of resource allocation to rhizobia thus prevents this interaction from becoming parasitic even in low-light, high-nitrogen environments where carbon is costly and nitrogen is readily available.

Microbial nitrogen fixation and methane oxidation are strongly enhanced by light in Sphagnum mosses

“…Three times higher microbial N 2 fixation rates and five times higher CH 4 oxidation rates in the presence of light indicate that these processes are strongly stimulated by photosynthesis, either directly or indirectly. For leguminous plant species it has recently been reported that the plants modulate their carbon allocation to symbiotic nitrogen-fixing Rhizobia in response to both light an N availability (Friel and Friesen 2019). For N 2 fixation associated with Sphagnum, it has been observed before that N 2 fixation rates are highest under illuminated conditions (Larmola et al 2014;van den Elzen et al 2017).…”

Biomass partitioning in response to intraspecific competition depends on nutrients and species characteristics: A study of 43 plant species

“…Gibert et al., 2019). This rhizobia–legume interaction strongly depends on the environment (Araújo et al., 2015; Batstone et al., 2020; Heath et al., 2010; Rehling et al., 2019; Zahran, 1999), but is particularly beneficial at high light, but low nutrient conditions (Friel & Friesen, 2019; Lau et al., 2012; Taylor & Menge, 2018). Second, the life span of a plant represents a trade‐off between survival and reproduction (Friedman, 2020) that affects its biomass allocation and response to different environments (Eziz et al., 2017; Husáková et al., 2018; Poorter et al., 2015).…”

How do less‐expensive nitrogen alternatives affect legume sanctions on rhizobia?

“…Furthermore, the severity of sanctions –the relative fitness between sanctioned and unsanctioned nodules–could depend on environmental conditions, such as fertilizer nitrogen in the soil, to which even legume crops are often exposed because of carry‐over from previous nonfixing crops. When soil nitrogen increases, legumes typically allocate fewer resources toward the symbiosis (Streeter & Wong, 1988; Denison & Harter, 1995; Fujikake et al., 2002; Friel & Friesen, 2019), although there are exceptions among legume species (Regus et al, 2014). But we understand less about the extent to which plants are capable of preferentially allocating resources to reflect the relative performance of each effective nodule on the same plant, sometimes called “relative sanctions” (West, Kiers, Simms, & Denison, 2002), which will play a large role in the evolutionary maintenance of the mutualism in today's changing terrestrial ecosystem.…”