Eric J. W. Visser

Interactions between Ethylene and Gibberellins in Phytochrome-Mediated Shade Avoidance Responses in Tobacco

Plants respond to proximate neighbors with a suite of responses that comprise the shade avoidance syndrome. These phytochrome-mediated responses include hyponasty (i.e. a more vertical orientation of leaves) and enhanced stem and petiole elongation. We showed recently that ethylene-insensitive tobacco (Nicotiana tabacum) plants (Tetr) have reduced responses to neighbors, showing an important role for this gaseous plant hormone in shade avoidance. Here, we investigate interactions between phytochrome signaling and ethylene action in shade avoidance responses. Furthermore, we investigate if ethylene acts in these responses through an interaction with the GA class of hormones. Low red to far-red light ratios (R:FR) enhanced ethylene production in wild-type tobacco, resulting in shade avoidance responses, whereas ethylene-insensitive plants showed reduced shade avoidance responses. Plants with inhibited GA production showed hardly any shade avoidance responses at all to either a low R:FR or increased ethylene concentrations. Furthermore, low R:FR enhanced the responsiveness of hyponasty and stem elongation in both wild-type and Tetr plants to applied GA3, with the stem elongation process being more responsive to GA3 in the wild type than in Tetr. We conclude that phytochrome-mediated shade avoidance responses involve ethylene action, at least partly by modulating GA action.

An Ethylene-Mediated Increase in Sensitivity to Auxin Induces Adventitious Root Formation in Flooded Rumex palustris Sm

The hormonal regulation of adventitious root formation induced by flooding of the root system was investigated in the wetland species Rumex palustris Sm. Adventitious root development at the base of the shoot is an important adaptation to flooded conditions and takes place soon after the onset of flooding. Decreases in either endogenous auxin or ethylene concentrations induced by application of inhibitors of either auxin transport or ethylene biosynthesis reduced the number of adventitious roots formed by flooded plants, suggesting an involvement of these hormones in the rooting process. The rooting response during flooding was preceded by increased endogenous ethylene concentrations in the root system. The endogenous auxin concentration did not change during flooding-induced rooting, but a continuous basipetal transport of auxin from the shoot to the rooting zone appeared to be essential in maintaining stable auxin concentrations. These results suggest that the higher ethylene concentration in soil-flooded plants increases the sensitivity of the root-forming tissues to endogenous indoleacetic acid, thus initiating the formation of adventitious roots.

A modular concept of plant foraging behaviour: the interplay between local responses and systemic control

In this paper we examined the notion that plant foraging for resources in heterogeneous environments must involve: (1) plasticity at the level of individual modules in reaction to localized environmental signals; and (2) the potential for modification of these responses either by the signals received from connected modules that may be exposed to different conditions, or by the signals reflecting the overall resource status of the plant. A conceptual model is presented to illustrate how plant foraging behaviour is achieved through these processes acting in concert, from the signal reception through signal transduction to morphological or physiological response. Evidence to support the concept is reviewed, using selective root placement under nutritionally heterogeneous conditions and elongation responses of stems and petioles to shade as examples. We discussed how the adoption of this model can promote understanding of the ecological significance of foraging behaviour. We also identified a need to widen the experimental repertoires of both molecular physiology and ecology in order to increase our insight into both the regulation and functioning of foraging responses, and their relationship with the patterns of environmental heterogeneity under which plants have evolved.

Shade tolerance: when growing tall is not an option

Two different plant strategies exist to deal with shade: shade avoidance and shade tolerance. All shade-exposed plants optimize photosynthesis to adapt to the decrease in light quality and quantity. When shaded, most species in open habitats express the shade-avoidance syndrome, a growth response to escape shade. Shade-tolerant species from forest understories cannot outgrow surrounding trees and adopt a tolerance response. Unlike shade avoidance, virtually nothing is known about regulation of shade tolerance. In this opinion article, we discuss potential modes of molecular regulation to adopt a shade-tolerance rather than a shade-avoidance strategy. We argue that molecular approaches using model and non-model species should help identify the molecular pathways that underpin shade tolerance, thus providing knowledge for further crop improvement.

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

Gas exchange between the plant and the environment is severely hampered when plants are submerged, leading to oxygen and energy deficits. A straightforward way to reduce these shortages of oxygen and carbohydrates would be continued photosynthesis under water, but this possibility has received only little attention. Here, we combine several techniques to investigate the consequences of anatomical and biochemical responses of the terrestrial species Rumex palustris to submergence for different aspects of photosynthesis under water. The orientation of the chloroplasts in submergence-acclimated leaves was toward the epidermis instead of the intercellular spaces, indicating that underwater CO2 diffuses through the cuticle and epidermis. Interestingly, both the cuticle thickness and the epidermal cell wall thickness were significantly reduced upon submergence, suggesting a considerable decrease in diffusion resistance. This decrease in diffusion resistance greatly facilitated underwater photosynthesis, as indicated by higher underwater photosynthesis rates in submergence-acclimated leaves at all CO2 concentrations investigated. The increased availability of internal CO2 in these “aquatic” leaves reduced photorespiration, and furthermore reduced excitation pressure of the electron transport system and, thus, the risk of photodamage. Acclimation to submergence also altered photosynthesis biochemistry as reduced Rubisco contents were observed in aquatic leaves, indicating a lower carboxylation capacity. Electron transport capacity was also reduced in these leaves but not as strongly as the reduction in Rubisco, indicating a substantial increase of the ratio between electron transport and carboxylation capacity upon submergence. This novel finding suggests that this ratio may be less conservative than previously thought.

Natural variation of submergence tolerance among arabidopsis thaliana accessions

• The exploitation of natural variation in Arabidopsis thaliana (Arabidopsis) provides a huge potential for the identification of the molecular mechanisms underlying this variation as a result of the availability of a vast array of genetic and genomic resources for this species. Eighty-six Arabidopsis accessions were screened for natural variation in flooding tolerance. This forms the first step towards the identification and characterization of the role of candidate genes contributing to flooding tolerance. • Arabidopsis accessions at the 10-leaf stage were subjected to complete submergence in the dark. Survival curves were plotted to estimate median lethal times as a measure of tolerance. Flooding-associated survival parameters, such as root and shoot oxygen content, initial carbohydrate content and petiole elongation under water, were also measured. • There was a significant variation in submergence tolerance among Arabidopsis accessions. However, the order of tolerance did not correlate with root and shoot oxygen content or initial amounts of shoot starch and total soluble sugars. A negative correlation was observed between submergence tolerance and underwater petiole elongation. • Arabidopsis accessions show considerable variation in the ability to tolerate complete submergence, making it a good species in which to identify and characterize genes and to study mechanisms that contribute to survival under water.

Acclimation to soil flooding - sensing and signal-transduction

Flooding results in major changes in the soil environment. The slow diffusion rate of gases in water limits the oxygen supply, which affects aerobic root respiration as well as many (bio)geochemical processes in the soil. Plants from habitats subject to flooding have developed several ways to acclimate to these growth-inhibiting conditions, ranging from pathways that enable anaerobic metabolism to specific morphological and anatomical structures that prevent oxygen shortage. In order to acclimate in a timely manner, it is crucial that a flooding event is accurately sensed by the plant. Sensing may largely occur in two ways: by the decrease of oxygen concentration, and by an increase in ethylene. Although ethylene sensing is now well understood, progress in unraveling the sensing of oxygen has been made only recently. With respect to the signal-transduction pathways, two types of acclimation have received most attention. Aerenchyma formation, to promote gas diffusion through the roots, seems largely under control of ethylene, whereas adventitious root development appears to be induced by an interaction between ethylene and auxin. Parts of these pathways have been described for a range of species, but a complete overview is not yet available. The use of molecular-genetic approaches may fill the gaps in our knowledge, but a lack of suitable model species may hamper further progress.

Two Rumex Species from Contrasting Hydrological Niches Regulate Flooding Tolerance through Distinct Mechanisms

Rumex palustris and Rumex acetosa are two closely related species that survive flooding using distinct strategies. Using a genomics approach, this study identifies novel molecular components and processes that contribute to the survival of these plant species that normally complete their life cycle in flood-prone environments. Global climate change has increased flooding events, which affect both natural vegetation dynamics and crop productivity. The flooded environment is lethal for most plant species because it restricts gas exchange and induces an energy and carbon crisis. Flooding survival strategies have been studied in Oryza sativa, a cultivated monocot. However, our understanding of plant adaptation to natural flood-prone environments remains scant, even though wild plants represent a valuable resource of tolerance mechanisms that could be used to generate stress-tolerant crops. Here we identify mechanisms that mediate the distinct flooding survival strategies of two related wild dicot species: Rumex palustris and Rumex acetosa. Whole transcriptome sequencing and metabolite profiling reveal flooding-induced metabolic reprogramming specific to R. acetosa. By contrast, R. palustris uses the early flooding signal ethylene to increase survival by regulating shade avoidance and photomorphogenesis genes to outgrow submergence and by priming submerged plants for future low oxygen stress. These results provide molecular resolution of flooding survival strategies of two species occupying distinct hydrological niches. Learning how these contrasting flood adaptive strategies evolved in nature will be instrumental for the development of stress-tolerant crop varieties that deliver enhanced yields in a changing climate.

Contrasting root behaviour in two grass species: a test of functionality in dynamic heterogeneous conditions

Root systems are highly plastic as they express a range of responses to acquire patchily distributed nutrients. However, the ecological significance of placing roots selectively in nutrient hotspots is still unclear. Here, we investigate under what conditions selective root placement may be a significant functional trait that determines belowground competitive ability. We studied two grasses differing in root foraging behaviour, Festuca rubra and Anthoxanthum odoratum. The plants were grown in stable and more dynamic heterogeneous environments, by switching nutrient patches halfway through the experiment. A. odoratum was a factor of two less selective in placing its roots into nutrient-rich patches than F. rubra. A. odoratum produced overall higher root length densities with higher specific root length than F. rubra and acquired more nutrients. A. odoratum appeared to be the superior competitor, irrespective of the nutrient dynamics. Our results suggest that root behaviour consisting of producing high root length densities at relatively low biomass investments can be a more effective foraging strategy than placing roots selectively in nutrient hotspots. When understanding the functionality of root traits among different species, specific root length may play a key role.

Zero methane emission bogs: extreme rhizosphere oxygenation by cushion plants in Patagonia

• Vascular wetland plants may substantially increase methane emissions by producing root exudates and easily degradable litter, and by providing a low-resistance diffusion pathway via their aerenchyma. However, model studies have indicated that vascular plants can reduce methane emission when soil oxygen demand is exceeded by oxygen released from roots. Here, we tested whether these conditions occur in bogs dominated by cushion plants. • Root-methane interactions were studied by comparing methane emissions, stock and oxygen availability in depth profiles below lawns of either cushion plants or Sphagnum mosses in Patagonia. • Cushion plants, Astelia pumila and Donatia fascicularis, formed extensive root systems up to 120 cm in depth. The cold soil (< 10°C) and highly decomposed peat resulted in low microbial activity and oxygen consumption. In cushion plant lawns, high soil oxygen coincided with high root densities, but methane emissions were absent. In Sphagnum lawns, methane emissions were substantial. High methane concentrations were only found in soils without cushion plant roots. • This first methane study in Patagonian bog vegetation reveals lower emissions than expected. We conclude that cushion plants are capable of reducing methane emission on an ecosystem scale by thorough soil and methane oxidation.