Genetic variation in tree leaf chemistry predicts the abundance and activity of autotrophic soil microorganisms

Abstract

Genetic variation in the chemistry of plant leaves can have ecosystem-level consequences.Here, we address the hypothesis that genetic variation in foliar condensed tannins along a Populus hybridization gradient influences soil ammonia oxidizers, a group of autotrophic microorganisms that perform the first step of nitrification and are not dependent on carbon derived from plant photosynthesis. Evidence that genetically based plant traits influence the abundance and activity of autotrophic soil microbes would greatly expand the concept of extended plant phenotypes. We found that increasing foliar condensed tannin concentration reduced rates of soil nitrification potential by~75%, reduced the abundance of ammonia-oxidizing archaea by~66%, but had no effect on ammonia-oxidizing bacteria. Other indices that often drive nitrification rates, including soil total nitrogen, foliar nitrogen, and soil pH, were not significant predictors of either the activity or the abundance of ammonia oxidizers, suggesting genetic variation in foliar condensed tannins may be the dominant regulating factor. These results demonstrate the condensed tannin phenotypes of two different tree species and their naturally occurring hybrids have extended effects on a key ecosystem process and provide evidence for indirect genetic linkages among autotrophs across at least two domains of life.

Tree genotypes affect rock lichens and understory plants: examples of trophic‐independent interactions

“…Genetic variation tends to enhance diversity and productivity, stabilize ecosystem functions, and stimulate positive plant–soil interactions (Genung et al 2010 , Keith et al 2010 , Crutsinger 2016 ). Genetic variation in a foundation species has been shown to influence the ecology, dynamics, and evolution of associated dependent species and communities (Evans et al 2008 , Gehring et al 2017 , Whitham et al 2020 ), and even extend to impact understory communities of vascular plants, autotrophic soil microorganisms, and epiphytic lichens (Adams et al 2011 , Lamit et al 2011a , 2011b , 2015 b , Al Hayek et al 2015 , Selmants et al 2019 ). These studies suggest that genetic variation in a foundation species can modify associated habitats and thus alter the composition of communities that do not rely on the foundation species for energy.…”

“…Although genetic variation in foundation species can influence species and communities that depend directly on the foundation species for a source of energy, the extent and manner in which this influence reaches organisms on the same trophic level remains poorly understood. A few studies on this topic have focused on Populus angustifolia James, P. fremontii S. Watson, and their hybrids, among which communities of understory vascular plants, epiphytic lichens, and autotrophic soil microorganisms differed (Adams et al 2011 , Lamit et al 2011a , 2011b , Selmants et al 2019 ). The fact that genetic variation in a foundation species can influence organisms on the same trophic level has important implications for ecological processes, such as community stability and nutrient cycling (Rudgers and Maron 2003 , Lankau and Strauss 2007 , Keith et al 2017 ).…”

Potential benefits of tanniferous forages in integrative crop-livestock agroecosystems

“…Interactions between soil microorganisms and tannins that affect organic matter formation and nutrient cycling are complex and influenced by the characteristics of the tannins (Fierer et al, 2001;Kraus et al, 2004;Norris et al, 2011;Schmidt et al, 2013b), plant genetics (Schweitzer et al, 2005;Schweitzer et al, 2008;Selmants et al, 2019), and may vary among different soil microbial groups (e.g. Souto et al, 2000;Selvakumar et al, 2007;Ushio et al, 2013;Zhang and Laanbroek, 2020).…”

Effects of phenotypic variation on consumer coexistence and prey community structure

“…For example, trait diversity within consumer species can have direct impacts on prey community composition as well as indirect effects on community primary productivity via trophic cascades[1–3]. Likewise, phenotypic trait diversity in host plant species can affect the composition of the host-associated microbiome and associated nutrient remineralization processes[4–6]. Intraspecific trait variability accounts for one-fourth of trait variability in natural plant communities[7] and can have ecological consequences that are comparable in magnitude to those from different species[8].…”