Community recommendations on terminology and procedures used in flooding and low oxygen stress research

Sasidharan, Rashmi; Bailey‐Serres, Julia; Ashikari, Motoyuki; Atwell, Brian J.; Colmer, Timothy D.; Fagerstedt, Kurt; Fukao, T.; Geigenberger, Peter; Hebelstrup, Kim H.; Hill, Robert D.; Holdsworth, Michael J.; Ismail, Abdelbagi M.; Licausi, Francesco; Mustroph, Angelika; Nakazono, Mikio; Pedersen, Ole; Perata, Pierdomenico; Sauter, Margret; Shih, Ming Che; Sorrell, Brian K.; Striker, Gustavo G.; Dongen, Joost T. van; Whelan, James; Xiao, Shi; Visser, Eric J. W.; Voesenek, Laurentius A. C. J.

doi:10.1111/nph.14519

Cited by 182 publications

(120 citation statements)

References 34 publications

(44 reference statements)

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“…In a plant that is subjected to submergence, this elevation is likely to occur in a transient fashion; however, as ROS formation from oxygen becomes chemically implausible when oxygen availability is strongly reduced and even impossible under bona fide anoxia, i.e. the complete absence of oxygen (Sasidharan et al, 2017). A sustained increase in ROS production as observed in different plant species (Yan et al, 1996;Liu et al, 2012a;Vergara et al, 2012) is unlikely to originate from the mitochondria and more likely the result of respiratory burst NADPH oxidase activity at the plasma membrane.…”

Section: Which Molecules Qualify As Upstream Mitochondrial Signals? Rmentioning

confidence: 99%

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

et al. 2018

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ORCID IDs: 0000-0001-5369-7911 (S.W.); 0000-0003-4024-968X (O.V.A.); 0000-0003-0796-8308 (M.S.).Cells of complex organisms typically rely on mitochondria for energy provision. The amount of energy required to sustain cellular activity can vary strongly depending on external conditions. Vice versa, constraints on respiratory activity due to metabolic status or stress insult require mitochondrial signaling to coordinate cellular physiology with the function of the organelle. In this update, we review recent insights into plant mitochondrial energy signaling in the light of their significance to stress acclimation. First, we focus on the characteristic adjustments of the nuclear transcriptome that occur after pharmacological inhibition of the mitochondrial electron transport chain as the output of mitochondrial retrograde signaling. Second, we discuss the proteins that have recently been identified as regulators of the transcript responses and the emerging picture of their action as a signaling network. We then pose the question of how well our current models of inducing mitochondrial dysfunction relate to conditions that plants face naturally. We reason that low-oxygen stress shows striking similarities with electron transport inhibitors with respect to their impact on mitochondrial energy physiology upstream, as well as the cellular transcriptomic response. Finally, we highlight and discuss changes in mitochondrial physiology that are common to both stimuli as candidates for upstream signals. The aim of this update is to better define the physiological context in which mitochondrial signaling operates to provide new directions for future research. RESPONSES TO MITOCHONDRIAL ENERGY SIGNALING AT THE TRANSCRIPT LEVEL

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Section: Which Molecules Qualify As Upstream Mitochondrial Signals? Rmentioning

confidence: 99%

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

et al. 2018

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“…The growth angle of 119.8°at 1 g in the dark was taken from Figure 1C, that of 106°at 0 g in the dark was taken from Figure 10B, that of 99°at 21 g in the dark was taken from Figure 10, D and F, and that of 54.2°in white light + ethephon was taken from Figure 7B. submergence, ;30% of the leaves remained above the water surface (Sasidharan et al, 2017).…”

Section: Plant Materials and Growth Conditionsmentioning

confidence: 99%

Control of Adventitious Root Architecture in Rice by Darkness, Light, and Gravity

Lin

Sauter

2017

Plant Physiol.

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ORCID IDs: 0000-0002-3607-6133 (C.L.); 0000-0002-7370-643X (M.S.).Rice (Oryza sativa) is a semiaquatic plant that is well adapted to partial flooding. Rice stems develop adventitious root (AR) primordia at each node that slowly mature but emerge only when the plant gets flooded, leading to the formation of a whole new secondary root system upon flooding. AR growth is induced by ethylene that accumulates in submerged plant tissues due to its lowered diffusion rate in water. Here, we report that the architecture of the secondary root system in flooded rice plants is controlled not only by altered gas diffusion but also by gravity and light. While ethylene promotes the emergence and growth of ARs, gravity and light determine their gravitropic setpoint angle (i.e. the deviation of growth direction relative to vertical). ARs grow upward at about 120°in the dark and downward at 54°in the light. The upward growth direction is conserved in indica and japonica rice varieties, suggestive of a conserved trait in rice. Experiments with a klinostat and with inverted stem orientation revealed that gravity promotes upward growth by about 10°. Red, far-red, and blue light lead to negative phototropism in a dose-dependent manner, with blue light being most effective, indicating that phytochrome and blue light signaling control AR system architecture. The cpt1 (coleoptile phototropism1) mutant, which lacks one of the phototropin-interacting CPT proteins, shows reduced sensitivity to blue light. Hence, the gravitropic setpoint angle of rice ARs is controlled by genetic and environmental factors that likely balance the need for oxygen supply (upward growth) with avoidance of root desiccation (downward growth).

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“…Floods are expected to increase in the coming decades in major wheat production areas due to climate change, increasing demand for the development of more flood‐tolerant wheat cultivars (Trnka et al, ). The terms “flooding” and “waterlogging” are often used interchangeably to describe excessively wet conditions, but in the following, we apply “waterlogging” only when the root zone is flooded and “submergence” when, in addition to the root system, all (or part of, i.e., partially submerged) the aboveground organs are under water (c.f., Sasidharan et al, ). In the present study, we tested if submergence tolerance in two contrasting wheat cultivars was related to levels of shoot carbohydrates as seen in rice ( Oryza sativa ; Das, Sarkar, & Ismail, ; Singh, Singh, & Ram, ) or governed by other traits.…”

Section: Introductionmentioning

confidence: 99%

Physiology, gene expression, and metabolome of two wheat cultivars with contrasting submergence tolerance

Herzog

Fukao

Winkel

et al. 2018

Plant Cell & Environment

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Responses of wheat (Triticum aestivum) to complete submergence are not well understood as research has focused on waterlogging (soil flooding). The aim of this study was to characterize the responses of 2 wheat cultivars differing vastly in submergence tolerance to test if submergence tolerance was linked to shoot carbohydrate consumption as seen in rice. Eighteen-day-old wheat cultivars Frument (intolerant) and Jackson (tolerant) grown in soil were completely submerged for up to 19 days while assessing responses in physiology, gene expression, and shoot metabolome. Results revealed 50% mortality after 9.3 and 15.9 days of submergence in intolerant Frument and tolerant Jackson, respectively, and significantly higher growth in Jackson during recovery. Frument displayed faster leaf degradation as evident from leaf tissue porosity, chlorophyll , and metabolomic fingerprinting. Surprisingly, shoot soluble carbohydrates, starch, and individual sugars declined to similarly low levels in both cultivars by day 5, showing that cultivar Jackson tolerated longer periods of low shoot carbohydrate levels than Frument. Moreover, intolerant Frument showed higher levels of phytol and the lipid peroxidation marker malondialdehyde relative to tolerant Jackson. Consequently, we propose to further investigate the role of ethylene sensitivity and deprivation of reactive O species in submerged wheat.

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Community recommendations on terminology and procedures used in flooding and low oxygen stress research

Cited by 182 publications

References 34 publications

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

Control of Adventitious Root Architecture in Rice by Darkness, Light, and Gravity

Physiology, gene expression, and metabolome of two wheat cultivars with contrasting submergence tolerance

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