Diversity, evolution, and function of stomata bearing structures in Cuscuta (dodders, Convolvulaceae): From extrafloral nectar secretion to transpiration in arid conditions

Courtney Clayson, Ignacio García-Ruiz, Mihai Costea

Research output: Contribution to journalArticle

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Abstract

Cuscuta includes ca. 200 species of functionally holoparasitic plants grouped in four subgenera: Monogynella, Cuscuta, Pachystigma, and Grammica. Multicellular structures with stomata in Cuscuta are represented by extrafloral nectaries (ENs), reported from the stems of one Monogynella species, and stomatiferous protuberances (SPs), which are non-secretory. These latter structures had been noted on the stems of three Grammica species more than a century ago but entirely forgotten until recently when similar, non-secretory SPs were reported on the flowers of several new Grammica species. Here we study for the first time: (1) the extent of occurrence, diversity and evolution of secretory (ENs) and non-secretory (SPs) multicellular structures in Cuscuta, and (2) the function of SPs. We undertook a character evolution study of ENs and SPs on the stems and flowers of 136 Cuscuta taxa, and examined the structure/ultrastructure of SPs. ENs are inferred as primitive and characterize subg. Monogynella. SPs are derived in the remaining subgenera; they are ubiquitous on the flowers of Cuscuta and Pachystigma, but absent on their stems. Subgenus Grammica species develop two functional types of stems during their life cycle: vegetative, exploratory stems with very low stomatal densities (and no SPs), and reproductive, haustorial stems with numerous SPs. Moreover, 24 species from nine clades of subg. Grammica have evolved morphologically diverse floral SPs with systematic significance. To preliminarily ascertain SP function, we determined in the field the water uptake of Tithonia tubiformis plants parasitized or not by Cuscuta costaricensis, a species with both stem and floral SPs, and the stomatal conductance of dodder stems and flowers, as well as host leaves. Water uptake of parasitized hosts was significantly higher compared to non-parasitized plants, even after host leaves were removed, both during the day and night. The increased water uptake of parasitized hosts and stomatal conductance values suggest a transpiration role for the SPs, which is also confirmed by their lacunar structure. Grammica species with floral SPs grow in arid areas or characterized by a pronounced dry season during flowering/fruiting, which suggests that SPs may have evolved to stimulate the host water uptake during these phenophases.

Original languageEnglish
Pages (from-to)310-321
Number of pages12
JournalPerspectives in Plant Ecology, Evolution and Systematics
Volume16
Issue number6
DOIs
StatePublished - 20 Dec 2014

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Keywords

  • Character evolution
  • Morphology
  • Nutrient acquisition
  • Stomata
  • Structure/ultrastructure
  • Transpiration

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