Research Article: Sucrose-induced stomatal closure is conserved across evolution

Date Published: October 12, 2018

Publisher: Public Library of Science

Author(s): Jayaram Kottapalli, Rakefet David-Schwartz, Belal Khamaisi, Danja Brandsma, Nitsan Lugassi, Aiman Egbaria, Gilor Kelly, David Granot, Carl Ng.

http://doi.org/10.1371/journal.pone.0205359

Abstract

As plants evolved to function on land, they developed stomata for effective gas exchange, for photosynthesis and for controlling water loss. We have recently shown that sugars, as the end product of photosynthesis, close the stomata of various angiosperm species, to coordinate sugar production with water loss. In the current study, we examined the sugar responses of the stomata of phylogenetically different plant species and species that employ different photosynthetic mechanisms (i.e., C3, C4 and CAM). To examine the effect of sucrose on stomata, we treated leaves with sucrose and then measured their stomatal apertures. Sucrose reduced stomatal aperture, as compared to an osmotic control, suggesting that regulation of stomata by sugars is a trait that evolved early in evolutionary history and has been conserved across different groups of plants.

Partial Text

The conquest of land by plants was an evolutionary process that began more than 450 million years ago [1]. Fossil, phylogenetic and molecular records indicate that the green algae and stoneworts (Charales) are probably the extant origin group of all land plants [2]. Extant land plants include three ‘non-vascular’ lineages, the liverworts, mosses and hornworts, collectively known as bryophytes. The remaining extant land plants are known as vascular plants (i.e., pteridophytes, gymnosperms and angiosperms), as they all possess complex water-conducting xylem tissue.

Stomatal opening is essential for CO2 uptake for photosynthesis and stomatal closure is necessary to reduce transpiration, maintain plant water potential and prevent desiccation. The coordination between photosynthesis and water loss has been fine-tuned by the evolution of mechanisms that open and close stomata. Passive hydration-dehydration guard-cell movements in ancient primitive plant species have evolved into sophisticated mechanisms activated by physiological and environmental signals, which lead to changes in the osmolyte content of guard cells and stomatal aperture. Light, CO2 concentration, vapor pressure deficit, temperature and water availability are among the environmental signals that affect stomatal movement [53, 54]. Yet, a direct effect of the primary product of photosynthesis, sucrose, on stomatal aperture has received little research attention over the years [55]. Red (photosynthetic) light opens stomata and mesophyll cells enhance stomatal opening, indicating that there is a mesophyll-derived product that opens stomata [56, 57]. Over the years, several studies have sought to identify the photosynthetic mesophyll product that opens stomata [56, 58] and sucrose, the obvious mesophyll-exported product, should have been be the primary mesophyll-derived candidate to be considered. Nevertheless, for many years, no functional study reported that sucrose opens stomata and two studies that did report an effect of sucrose found no opening effect and even a closing effect [59, 60]. We assume that those observations regarding the closure effect of sucrose were neglected because they ran counter to the prevailing hypothesis that sucrose is an osmolyte that opens stomata.

 

Source:

http://doi.org/10.1371/journal.pone.0205359

 

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