Allocating nitrogen away from a herbivore: a novel compensatory response to root herbivory

Abstract

Centaurea maculosa, an invasive North American plant species, shows a high degree of tolerance to the root-boring biocontrol herbivore, Agapeta zoegana. For example, infested individuals of C. maculosa often exhibit more rigorous growth and reproduction compared with their non-infested counterparts. Compensatory responses to aboveground herbivores often involve increases in leaf area and/or photosynthetic capacity, but considerably less is known about root system compensatory responses to belowground herbivory. We used a (15)N labeling approach to evaluate whether compensatory adjustments in N acquisition via changes in root morphology and/or physiological uptake capacity could explain the ability of C. maculosa to tolerate root herbivory. Root herbivory reduced whole plant N uptake by more than 30% and root uptake capacity by about 50%. Despite a marked reduction in N procurement, herbivory did not affect total biomass or shoot N status. Infested plants maintained shoot N status by shifting more of the acquired N from the root to the shoot. To our knowledge, shifting N allocation away from a root herbivore has not been reported and provides a plausible mechanism for the host plant to overcome an otherwise devastating effect of a root herbivore-induced N deficit.

Temporal Changes in Allocation and Partitioning of New Carbon as 11C Elicited by Simulated Herbivory Suggest that Roots Shape Aboveground Responses in Arabidopsis

“…The rapid movement of resources belowground observed in our study is also in agreement with the growing body of literature demonstrating the transport of resources away from damaged sites and into roots and storage organs within hours following herbivory (Babst et al, , 2008Schwachtje et al, 2006;Newingham et al, 2007;Frost and Hunter, 2008;Kaplan et al, 2008;Gómez et al, 2010Gómez et al, , 2012. The adaptive value of sequestering resources to roots has been explained in various ways, including storing reserves for later regrowth to tolerate herbivory (Schwachtje et al, 2006).…”

“…Previous studies using this short-lived isotope have narrowed their focus to short-term dynamics in resource allocation occurring immediately (within hours) following herbivory. These experiments suggest that plants respond to leaf damage by rapidly transporting recently fixed carbon from both damaged and undamaged tissues to roots, a response thought to be employed by plants to tolerate herbivory by bunkering resources away from sites of damage and into storage belowground for later regrowth (Babst et al, , 2008Schwachtje et al, 2006;Newingham et al, 2007;Frost and Hunter, 2008;Kaplan et al, 2008;Gómez et al, 2010Gómez et al, , 2012Orians et al, 2011).…”

Ustilago maydis Infection Strongly Alters Organic Nitrogen Allocation in Maize and Stimulates Productivity of Systemic Source Leaves

“…In addition, it was recently observed that, upon infection of spotted knapweed (Centaurea maculosa) with the root herbivore Agapeta zoegana, total nitrogen uptake was reduced and nitrogen was translocated from the root to the shoot of the plant (Newingham et al, 2007). These examples suggest that plants have evolved a way of limiting nutrient supply at the infection site.…”

Why Does Herbivore Attack Reconfigure Primary Metabolism?

“…If plants are attacked by root herbivores, assimilates can be remobilized above ground. The highly tolerant Centaurea maculosa responds to root herbivory by the knapweed moth by reducing its nitrogen (N) uptake but also shifting N to aboveground tissues (Newingham et al, 2007), suggesting that N allocation can be a determinant of tolerance. This idea is supported by the finding that after its leaves were clipped, the dwarf shrub Indigofera spinosa increased its root N uptake (Coughenour et al, 1990) and that Quercus serrata accumulates higher N levels in leaves (Takashima et al, 2004).…”