Functional anatomy of haustoria formed by Rhinanthus minor: linking evidence from histology and isotope tracing

Abstract

Summary• The root parasite Rhinanthus minor feeds on the xylem of a diverse range of species. Grasses and legumes are the best hosts, while on forbs R. minor typically shows poorer growth. It has been hypothesized that host quality is linked to the expression of defences against the parasite seen in forb roots, but never in grasses. The efficacy of these defence mechanisms in preventing resource loss has not, however, been measured directly.• Here we combine histological characterization of haustoria formed on Cynosurus cristatus (a grass), Leucanthemum vulgare and Plantago lanceolata (forbs) with 15 N tracers supplied to the host to quantify the efficacy of these defence responses.• Rhinanthus minor penetrated only the xylem of C. cristatus , abstracting an average of 17% of the 15 N tracer taken up, but only 2.5 and 0.2%, respectively, when attached to L. vulgare and P. lanceolata .• For the first time, this study has established that the resistance mechanisms of the forbs are effective in preventing the parasite from directly accessing their xylem solutes.

Heterotrophic carbon gain by the root hemiparasites, Rhinanthus minor and Euphrasia rostkoviana (Orobanchaceae)

“…Xylem sap is generally assumed to contain only a minimal amount of organic carbon, but a recent investigation has revealed that organic compounds can constitute ca 50% of xylem solutes (Alvarez et al 2008) suggesting that the xylem is in fact a rich source of organic carbon for the parasite. Hence, the high rate of carbon heterotrophy in R. minor reported in our study is not surprising given its highly efficient abstraction of xylem solutes when attached to a suitable host (Jiang et al 2003;Cameron and Seel 2007). Substantial variability in the degree of heterotrophy observed amongst individual plants of R. minor might be in part explained by a positive feedback relationship between hemiparasite growth and the amount of xylem sap that it is able to abstract from the host's vascular system.…”

“…Direct luminal continuity between host and parasite vessel elements has been reported in R. minor haustoria (Cameron et al 2006;Cameron and Seel 2007;Rümer et al 2007). The uptake of xylem solutes is driven by mass flow because of the lower water potential of the parasite induced through the accumulation of osmotically active sugar alcohols (Jiang et al 2008a) and elevated parasite transpiration rates facilitated by permanently open stomata that are insensitive to ABA-induced closure (Jiang et al 2003).…”

“…The mixing model calculations suggest that on average, over 50% of leaf biomass of the experimental individuals consists of host-derived carbon, although the model outputs are highly variable. Rhinanthus minor is known to be very efficient in the extraction of solutes of the host xylem (Jiang et al 2003;Cameron and Seel 2007) due to an advanced haustorial structure (Cameron and Seel 2007;Rümer et al 2007). Moreover, infection by R. minor is certainly more detrimental (in terms of host growth and fecundity reduction) than most other temperate hemiparasites (Gibson and Watkinson 1992;Matthies 1995).…”

“…1). Although it has been demonstrated that P. lanceolata is resistant to R. minor (Cameron et al 2006;Rümer et al 2007) and the parasite is unable to abstract resources from this species (Cameron and Seel 2007), the design of the pot further decreases the probability of any interaction between R. minor and the reference plant. Pots were maintained in a controlled environment chamber with a cycle of 14-h light at 20°C and 10-h dark at 15°C (Conviron, Winnipeg, Canada).…”

Growth, survival and generative reproduction in a population of a widespread annual hemiparasite Melampyrum pratense

“…This suggests that the total reproductive output and hence also fitness is dependent on vegetative growth across the whole lifespan. In this respect, it is quite likely that differential rate of early development are underpinned by quality of attachment to the host (Cameron & Seel 2007) since otherwise all individuals occur on the same site and the intensity of competition for light potentially affecting the seedlings in the spring period (Těšitel et al 2011) is minimal due to the very open forest understory.…”