The importance of aboveground–belowground interactions on the evolution and maintenance of variation in plant defense traits

Abstract

Over the past two decades a growing body of empirical research has shown that many ecological processes are mediated by a complex array of indirect interactions occurring between rhizosphere-inhabiting organisms and those found on aboveground plant parts. Aboveground–belowground studies have thus far focused on elucidating processes and underlying mechanisms that mediate the behavior and performance of invertebrates in opposite ecosystem compartments. Less is known about genetic variation in plant traits such as defense as that may be driven by above- and belowground trophic interactions. For instance, although our understanding of genetic variation in aboveground plant traits and its effects on community-level interactions is well developed, little is known about the importance of aboveground–belowground interactions in driving this variation. Plant traits may have evolved in response to selection pressures from above- and below-ground interactions from antagonists and mutualists. Here, we discuss gaps in our understanding of genetic variation in plant-related traits as they relate to aboveground and belowground multitrophic interactions. When metabolic resources are limiting, multiple attacks by antagonists in both domains may lead to trade-offs. In nature, these trade-offs may critically depend upon their effects on plant fitness. Natural enemies of herbivores may also influence selection for different traits via top–down control. At larger scales these interactions may generate evolutionary “hotspots” where the expression of various plant traits is the result of strong reciprocal selection via direct and indirect interactions. The role of abiotic factors in driving genetic variation in plant traits is also discussed.

Comparative proteomic analysis of oil palm leaves infected with Ganoderma boninense revealed changes in proteins involved in photosynthesis, carbohydrate metabolism, and immunity and defense

“…It has been hypothesized that when plant roots are exposed to belowground pathogens, defense responses are sent via a series of signaling molecules to the aboveground foliar. This has been demonstrated in several studies where responses triggered belowground were transported aboveground and vice versa to better prepare the plant for defense strategies . In oil palms, it has been shown that expression of defense‐related genes can be detected in both root and leaf tissues of Ganoderma ‐infected seedlings .…”

Metabolomics in plant–herbivore interactions: challenges and applications

“…In their natural environment, plants engage in interactions not only above but also belowground. Moreover, indirect interactions between soil‐borne and aerial organisms may be mediated by the plant itself (van Dam & Heil, ; van Geem et al., ). In the context of these plant‐mediated interactions across spatial scales, LC‐MS based metabolic fingerprinting, alongside targeted glucosinolate profiling and GC‐MS based quantitation of primary metabolites, was used to detect chemical changes in local and systemic tissues of A. thaliana plants infested by aphids (leaves), nematodes (roots), or both (Kutyniok & Müller, ).…”

Below‐ground nematode herbivory of resistant soybean cultivars impairs the performances of an above‐ground caterpillar and its parasitoid

“…However, a recent study in cotton showed that root herbivory by the gall‐forming root‐knot nematode M. incognita had no impact on the performance of the cotton herbivore H. zea , which ultimately had no effect on the attraction of the parasitoid Microplitis croceipes (Cresson) to their hosts (Olson et al ., ). Therefore, we are only beginning to scratch the surface in our understanding of above‐ and below‐ground interactions between herbivores and their natural enemies (van Geem et al ., ; van Veen, ).…”