Plant Hormones Regulate Fast Shoot Elongation Under Water: From Genes to Communities

Abstract

Flooding affects the abundance and distribution of plant species worldwide. Many plants are damaged or even killed by flooding events due to the associated oxygen deprivation in cells. Stimulated shoot elongation is an important adaptive mode that can restore contact of leaves with the atmosphere above the water surface. This strongly improves inward diffusion of oxygen and the rate of photosynthesis. Fast elongation of submerged petioles of the model plant Rumex palustris involves the integrated action of the plant hormones ethylene, auxin, gibberellin, and abscisic acid. The closely related Rumex acetosa is unable to switch on petiole elongation when submerged. In a comparative study of these two Rumex species, we found that the response to the gaseous phytohormone ethylene, which accumulates in plant tissues during submergence, explains their contrasting elongation behavior. In order to study the importance of this shoot elongation response in the distributional patterns of plants in natural floodplains, we quantified the ethylene‐induced elongation response of 22 plant species occurring in the Rhine River floodplain. These results were compared with the results of a multivariate analysis based on 84 vegetation surveys performed in the same area. The species compositions of the surveys were grouped along two environmental gradients: flooding duration and soil dehydration after the floodwater subsided. If we superimpose the ethylene‐induced elongation capacity on these vegetation data, it becomes clear that the capacity to elongate upon exposure to ethylene positively correlates with flooding duration and negatively with soil dehydration. Based on this analysis, we conclude that the capacity to elongate is an important selective trait in field distribution patterns of plants in flood‐prone environments. Fast shoot elongation under water seems to be a favorable trait only in environments with shallow and prolonged flooding events, while costs associated with this response prevent its expression in sites with deep floods, sites with floods short in duration, or in sites in which flood water recedes rapidly. The approach outlined in this paper may be more widely applicable in ecological studies that aim to understand the functional relationship between plant traits and species distributions along environmental gradients.

Anatomical and morphological modifications in response to flooding by six Cerrado tree species

“…However, when subjected to extended periods of flooding and the water column is relatively shallow, it may be more beneficial to the plant to undergo rapid shoot elongation to escape submersion. Some species rapidly elongate their stems or petioles keeping leaves above the water surface, facilitating gas exchange and light interception (Voesenek et al 2004;Kolb & Joly 2009;Manzur et al 2009;Chen et al 2010).…”

Biophysical probing of Spartina maritima photo-system II changes during prolonged tidal submersion periods

“…This photosynthetic impairment due to low CO 2 or low light, leads to a depletion in the O 2 production, with less O 2 to be diffused from the leaves to the roots, and thus increasing the anoxia driven stress at the sediment level (Colmer and Flowers, 2008). Moreover, plant feedback to flooding events will be also function of the duration and water column depth, and of course, plant genotype (Setter and Waters, 2003;Voesenek et al, 2004). Due to obvious geographical constrains, the species inhabiting the lower parts of coastal marshes are more exposed both to normal tidal flooding, but also to prolonged flooding events.…”

Submergence-Induced Morphological, Anatomical, and Biochemical Responses in a Terrestrial Species Affect Gas Diffusion Resistance and Photosynthetic Performance

“…This can lead to oxygen deficiency in the plant and, concomitantly, energy deficits due to hampered aerobic metabolism (Crawford and Brändle, 1996). Well-known adaptations of plants to submergence include elongation of shoot organs to restore contact with the atmosphere (Voesenek et al, 2004) and the ability to switch to anaerobic metabolism to generate ATP in the absence of O 2 (Perata and Alpi, 1993). Another, yet overlooked, phenomenon to reduce the shortages of oxygen and carbohydrates might be the potential for sustained photosynthesis under water (He et al, 1999;Vervuren et al, 1999).…”