Ultrastructure of hydathode trichomes of hemiparasitic Rhinanthus alectorolophus and Odontites vernus: how important is their role in physiology and evolution of parasitism in Orobanchaceae?

Abstract

The Rhinanthoid clade of the family Orobanchaceae comprises plants displaying a hemiparasitic or holoparasitic strategy of resource acquisition. Some of its species (mainly Rhinanthus spp.) are often used as models for studies of hemiparasite physiology. Although there is a well-developed concept covering their physiological processes, most recent studies have neglected the existence of hydathode trichomes present on leaves of these hemiparasitic plants. As a first step for the proposed integration of these structures in the theory of physiological processes of the hemiparasites, we described the outer micromorphology and ultrastructure of the hydathode trichomes on leaves of hemiparasitic Rhinanthus alectorolophus and Odontites vernus with scanning and transmission electron microscopy (SEM and TEM, respectively). The TEM inspections of both types of trichome revealed typical ultrastructural features: labyrinthine cell wall, high content of cytoplasm in cells with numerous mitochondria and presence of plasmodesmata. All these features indicate high metabolic activity complying with their function as glandular trichomes actively secreting water. The active secretion of water by the hydathode trichomes (evidence for which is summarised here) also presents a possible mechanism explaining results of previous gas exchange measurements detecting high dark respiration and transpiration rates and a tight inter-correlation between them in hemiparasitic Orobanchaceae. In addition, this process is hypothesised to have allowed multiple evolutionary transitions from facultative to obligate hemiparasitism and unique xylem-feeding holoparasitism of Lathraea with a long-lived underground stage featuring a rhizome covered by scales of leaf origin.

Integrating ecology and physiology of root‐hemiparasitic interaction: interactive effects of abiotic resources shape the interplay between parasitism and autotrophy

“…The contrasting outcomes of the hemiparasitic interaction described earlier are based simply on quantitative adjustments of physiological processes that are well known to occur in root hemiparasites. Despite infecting its hosts below ground, parasitic resource acquisition in Rhinanthus is mostly driven by the shoot, which contains osmotically active sugar alcohols (Jiang et al ., ), displays a high transpiration rate (Klaren & van de Dijk, ; Jiang et al ., ) and can even actively secrete water by hydathode trichomes (Govier et al ., ; Těšitel & Tesařová, ), together generating a water potential gradient between host and Rhinanthus and so facilitating mass flow of nutrients to the parasite. The hemiparasite maintains this water potential difference, directing resource flow from the host through open vascular connections in the haustoria (Jiang et al ., ; Cameron et al ., ).…”

“…Typical hemiparasites withdraw resources exclusively from host xylem, while holoparasites have access to host phloem as well as the xylem (Irving & Cameron, ), although exceptions and intermediate forms exist. These include the xylem‐only feeding holoparasitic genus Lathraea (Ziegler, ; Těšitel & Tesařová, ) and the largely heterotrophic phloem‐feeding genus Cuscuta , which retains limited photosynthetic capacity (Hibberd et al ., ; Švubová et al ., ). Hemiparasites constitute c .…”

A hemiparasite in the forest understorey: photosynthetic performance and carbon balance ofMelampyrum pratense

“…However, values of stomatal conductance cannot be calculated from transpiration in M. pratense and several related root hemiparasites from Orobanchaceae as they have specialised hydathode trichomes that secrete water from leaves (Fedorowicz ; Govier et al . ; Weber ; Kubát & Weber ; Těšitel ; Těšitel & Tesařová ; Světlíková et al . ).…”

Glandular trichomes on the leaves and flowers of Bellardia trixago and Parentucellia viscosa (Orobanchaceae)

“…The mucilage of long-stalked capitate trichomes may play an important adaptive role in the xeric Mediterranean environments and may also act as chemical defense against herbivores and pathogens. Short-stalked trichomes are probably hydathodes excreting actively water, function that was recently recognized to the similar trichomes of Odontites vernus [6]. Further studies are needed to confirm the role of these glandular trichomes in hemparasitic species.…”