Transcriptomic responses to conspecific and congeneric competition in co‐occurring Trifolium

Abstract

1. Species coexistence requires differential response to inter-and intraspecific competition, typically conceptualized as niche differentiation. Coexistence of close relatives therefore poses an interesting scenario with regards to niche differentiation since these species generally have many traits in common due to shared ancestry. Native Californian Trifolium assemblages are locally diverse and represent a unique system for understanding competitive interactions among close relatives.2. We conducted two similar greenhouse studies in which Trifolium fucatum was grown alone, with a conspecific competitor, and with a congeneric competitor (Trifolium macraei). In the first study, we assessed biomass production in T. fucatum, and in the second study we conducted an RNAseq analysis of T. fucatum roots to test for differentially expressed genes that may mediate competitive interactions and potentially coexistence.3. Compared to plants grown alone, competition (i.e. growth in the same pot) with a conspecific resulted in a greater reduction in biomass than competition with a congener, as predicted by theory. However, competition with a congener resulted in twice as many differentially expressed genes as competition with a conspecific. 4.Annotations of identified genes differentiating congeneric from conspecific competition suggest several functions attributed to interactions with third-party organisms, including nodulation with rhizobial mutualists, and defence responses against pathogens and herbivores. In addition, salt-responsive genes and an iron transporter were differentially expressed in congeneric competition, and comparisons of sodium and iron concentrations in field soils where these species are found showed that T. fucatum occurs in higher sodium and iron microsites than T. macraei. Thus, the transcriptome highlighted abiotic niche axes worth pursuing in future ecological experiments as potential mediators of coexistence. 5.We also found a subset of genes that responded similarly to both congeneric and conspecific competition in both direction and magnitude, indicating some conserved responses to competition, regardless of neighbour identity. 6. Synthesis. Transcriptomic analyses represent novel tools for identifying the molecular mechanisms underlying interactions among species. Working iteratively with ecological experimentation and observation, transcriptomes may allow us to identify novel dimensions of the n-dimensional niche that determine species' distributions and their ability to coexist.

The genetics underlying natural variation of plant–plant interactions, a beloved but forgotten member of the family of biotic interactions

“…Ethylene‐related genes were up‐regulated in Trifolium fucatum when competing with its congeneric T . macraei (Bowsher et al ., ). In addition, two candidates underlying two other QTLs of response to inter‐genotypic competition in A .…”

“…thaliana , two studies reported an up‐regulation of defense‐related genes (Biedrzycki et al ., ; Masclaux et al ., ), while a third study reported the opposite pattern (Geisler et al ., ). Up‐regulation and down‐regulation of defense‐related genes were even reported within the same studies (Horvath et al ., ; Bowsher et al ., ). The growth‐defense balance theory predicts that light perception by photoreceptors activates SAS and reduces the expression of defenses against microbial pathogens and insects, by a simultaneous down‐regulation of jasmonate and salicylic acid signaling (Ballaré, ; Ballaré and Pierik, ).…”

“…In competition with conspecifics, auxin-related genes were upregulated in barley and maize (St. Pierre et al, 2011;Choe et al, 2016) and a subunit (ASA1) of anthranilate synthase, which is involved in auxin synthesis, was proposed as a candidate gene underlying a QTL of response to inter-genotypic competition in A. thaliana (Mutic and Wolf, 2007). Ethylene-related genes were up-regulated in Trifolium fucatum when competing with its congeneric T. macraei (Bowsher et al, 2017). In addition, two candidates underlying two other QTLs of response to inter-genotypic competition in A. thaliana correspond to two polypeptides (ACS4 and ACS10) involved in the formation of 1-amino-cyclopropane-1-carboxylate synthase (ACS), which governs the rate-limiting step in ethylene formation (Mutic and Wolf, 2007).…”

“…Cell wall modification and degradation are important components of cell expansion, which is the driving force of organ elongation (Ballar e and Pierik, 2017). In line with the cell growth machinery being the ultimate target of the signal transduction network involved in SAS and hormonerelated pathways, genes related to cell wall modification and degradation were up-regulated in presence of intraspecific competition (Choe et al, 2016;Bowsher et al, 2017). A genomic region of less than 10 kb associated with the length of reproductive period in A. thaliana has been fine mapped in response to the presence of Stellaria media (Baron et al, 2015).…”

“…The growth-defense balance theory predicts that light perception by photoreceptors activates SAS and reduces the expression of defenses against microbial pathogens and insects, by a simultaneous down-regulation of jasmonate and salicylic acid signaling (Ballar e, 2014;Ballar e and Pierik, 2017). While some transcriptomic studies support this trade-off (Schmidt and Baldwin, 2006;Geisler et al, 2012), other studies suggest an independent regulation of the SAS-related pathways and defense pathways in the focal plant competing with a neighbor plant (Masclaux et al, 2012;Horvath et al, 2015;Bowsher et al, 2017). Accordingly, some recent studies documented a reduction of disease severity in focal plants that were challenged by neighbor plants (Figure 3).…”