Localized Hormone Fluxes and Early Haustorium Development in the Hemiparasitic Plant Triphysaria versicolor

Abstract

Perhaps the most obvious phenotypes associated with chemical signaling between plants are manifested by parasitic species of Orobanchaceae. The development of haustoria, invasive root structures that allow hemiparasitic plants to transition from autotrophic to heterotrophic growth, is rapid, highly synchronous, and readily observed in vitro. Haustorium development is initiated in aseptic roots of the facultative parasite Triphysaria versicolor when exposed to phenolic molecules associated with host root exudates and rhizosphere bioactivity. Morphological features of early haustorium ontogeny include rapid cessation of root elongation, expansion, and differentiation of epidermal cells into haustorial hairs, and cortical cell expansion. These developmental processes were stimulated in aseptic T. versicolor seedlings by the application of exogenous phytohormones and inhibited by the application of hormone antagonists. Surgically dissected root tips formed haustoria if the root was exposed to haustorial-inducing factors prior to dissection. In contrast, root tips that were dissected prior to inducing-factor treatment were unable to form haustoria unless supplemented with indole-3-acetic acid. A transient transformation assay demonstrated that auxin and ethylene-responsive promoters were up-regulated when T. versicolor was exposed to either exogenous hormones or purified haustoria-inducing factors. These experiments demonstrate that localized auxin and ethylene accumulation are early events in haustorium development and that parasitic plants recruit established plant developmental mechanisms to realize parasite-specific functions.It has been estimated that over 4,000 species of angiosperms are able to directly invade and parasitize other plants (Nickrent, 2003). Parasitic plant species have widely different hosts and habits, ranging from mistletoes that grow on the tops of conifer trees to root parasites that live most of their lives underground (Press and Graves, 1995). A single feature common to all parasitic plants is the ability to develop invasive structures called haustoria (Riopel and Timko, 1995). After invasion, parasitic plant haustoria function as physiological bridges through which the parasite robs host plants of water and nutrients. The competence to form haustoria is the defining characteristic of parasitic plants, distinguishing them from epiphytic and mycoheterotrophic plants that either use host plants for physical support or associate via mycorrhizal intermediates (Kuijt, 1969;Leake, 1994).It is clear from several lines of evidence that parasitic plants evolved from nonparasitic autotrophs (Kuijt, 1969). There are two general models for the evolutionary origins of the haustoria that define plant parasitism. One model proposes that genes encoding haustorium development are foreign to plants and were introduced into parasitic species via an endosymbiotic or horizontal gene transfer event, perhaps from a haustorial-producing fungus or bacteria (Atsatt, 1973). An alterative hypothesis proposes that gen...

Detection and Adaptation in Parasitic Angiosperm Host Selection

“…The general up-regulations of genes associated with nutrient metabolism and transport are consistent with the principal function of the haustorium: tapping host resources. The regulated flux of auxins and cytokinins is probably the most expected of a developmental transition and consistent with previous studies of haustorial organogenesis [22].…”

“…A role for auxin at this early time point is also consistent with the arrest of root elongation observed upon DMBQ exposure prior to commitment. Phytohormone studies in T. versicolor have also implicated a role for auxin signaling in haustorial organogenesis [22]. As cytokinins induce haustorium development, the developmental transition may also be regulated by both of these often antagonistic hormones [11].…”

De Novo Assembly and Characterization of the Transcriptome of the Parasitic Weed Dodder Identifies Genes Associated with Plant Parasitism

“…Polar auxin accumulation has been postulated as a universal feature of early plant organogenesis, and localized auxin accumulation has been shown to be required for early haustorium development in T. versicolor (Benková et al, 2003;Tomilov et al, 2005). An increased activity of genes underlying polar auxin transport in dodder infective stages likely establishes auxin maxima that induce haustoria formation.…”

Endogenous hormone levels and anatomical characters of haustoria in Santalum album L. seedlings before and after attachment to the host

“…In the aseptic roots of the facultative parasite Triphysaria versicolor, haustorial development can be initiated by exposing the roots to phenolic derivatives exuded by the hosts' roots (Albrecht et al, 1999). Tomilov et al (2005) identified the accumulation of auxin and ethylene as early events in haustorium development of the hemiparasitic plant T. versicolor. S. album seeds pretreated with 2-8 mM gibberellic acid (GA 3 ) for 12 h could germinate in vitro on Murashige and Skoog medium (Nikam and Barmukh, 2009).…”