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2.  Evolution and mechanisms of plant tolerance to flooding stress 
Annals of Botany  2009;103(2):137-142.
In recognition of the 200th anniversary of Charles Darwin's birth, this short article on flooding stress acknowledges not only Darwin's great contribution to the concept of evolution but also to the study of plant physiology. In modern biology, Darwin-inspired reductionist physiology continues to shed light on mechanisms that confer competitive advantage in many varied and challenging environments, including those where flooding is prevalent.
Mild flooding is experienced by most land plants but as its severity increases, fewer species are able to grow and survive. At the extreme, a highly exclusive aquatic lifestyle appears to have evolved numerous times over the past 120 million years. Although only 1–2% of angiosperms are aquatics, some of their adaptive characteristics are also seen in those adopting an amphibious lifestyle where flooding is less frequent. Lowland rice, the staple cereal for much of tropical Asia falls into this category. But, even amongst dry-land dwellers, or certain of their sub-populations, modest tolerance to occasional flooding is to be found, for example in wheat. The collection of papers summarized in this article describes advances to the understanding of mechanisms that explain flooding tolerance in aquatic, amphibious and dry-land plants. Work to develop more tolerant crops or manage flood-prone environments more effectively is also included. The experimental approaches range from molecular analyses, through biochemistry and metabolomics to whole-plant physiology, plant breeding and ecology.
PMCID: PMC2707321  PMID: 19145714
Abiotic stress; adaptation; anoxia; Charles Darwin; environmental stress; evolution; flooding; hypoxia; rice; submergence; wetlands
3.  Root signals and stomatal closure in relation to photosynthesis, chlorophyll a fluorescence and adventitious rooting of flooded tomato plants 
Annals of Botany  2008;103(2):313-323.
Background and Aims
An investigation was carried out to determine whether stomatal closure in flooded tomato plants (Solanum lycopersicum) results from decreased leaf water potentials (ψL), decreased photosynthetic capacity and attendant increases in internal CO2 (Ci) or from losses of root function such as cytokinin and gibberellin export.
Pot-grown plants were flooded when 1 month old. Leaf conductance was measured by diffusion porometry, the efficiency of photosystem II (PSII) was estimated by fluorimetry, and infrared gas analysis was used to determine Ci and related parameters.
Key Results
Flooding starting in the morning closed the stomata and increased ψL after a short-lived depression of ψL. The pattern of closure remained unchanged when ψ`L depression was avoided by starting flooding at the end rather than at the start of the photoperiod. Raising external CO2 concentrations by 100 µmol mol−1 also closed stomata rapidly. Five chlorophyll fluorescence parameters [Fq′/Fm′, Fq′/Fv′, Fv′/Fm′, non-photochemical quenching (NPQ) and Fv/Fm] were affected by flooding within 12–36 h and changes were linked to decreased Ci. Closing stomata by applying abscisic acid or increasing external CO2 substantially reproduced the effects of flooding on chlorophyll fluorescence. The presence of well-aerated adventitious roots partially inhibited stomatal closure of flooded plants. Allowing adventitious roots to form on plants flooded for >3 d promoted some stomatal re-opening. This effect of adventitious roots was not reproduced by foliar applications of benzyl adenine and gibberellic acid.
Stomata of flooded plants did not close in response to short-lived decreases in ψL or to increased Ci resulting from impaired PSII photochemistry. Instead, stomatal closure depressed Ci and this in turn largely explained subsequent changes in chlorophyll fluorescence parameters. Stomatal opening was promoted by the presence of well-aerated adventitious roots, implying that loss of function of root signalling contributes to closing of stomata during flooding. The possibility that this involves inhibition of cytokinin or gibberellin export was not well supported.
PMCID: PMC2707317  PMID: 19001430
Root to shoot communication; flooding stress; stomatal closure; photosynthesis; chlorophyll fluorescence; gas exchange; adventitious roots; plant hormones; abscisic acid; cytokinins; gibberellic acid
4.  Ethylene-promoted Elongation: an Adaptation to Submergence Stress 
Annals of Botany  2007;101(2):229-248.
A sizeable minority of taxa is successful in areas prone to submergence. Many such plants elongate with increased vigour when underwater. This helps to restore contact with the aerial environment by shortening the duration of inundation. Poorly adapted species are usually incapable of this underwater escape.
Evidence implicating ethylene as the principal factor initiating fast underwater elongation by leaves or stems is evaluated comprehensively along with its interactions with other hormones and gases. These interactions make up a sequence of events that link the perception of submergence to a prompt acceleration of extension. The review encompasses whole plant physiology, cell biology and molecular genetics. It includes assessments of how submergence threatens plant life and of the extent to which the submergence escape demonstrably improves the likelihood of survival.
Experimental testing over many years establishes ethylene-promoted underwater extension as one of the most convincing examples of hormone-mediated stress adaptation by plants. The research has utilized a wide range of species that includes numerous angiosperms, a fern and a liverwort. It has also benefited from detailed physiological and molecular studies of underwater elongation by rice (Oryza sativa) and the marsh dock (Rumex palustris). Despite complexities and interactions, the work reveals that the signal transduction pathway is initiated by the simple expediency of physical entrapment of ethylene within growing cells by a covering of water.
PMCID: PMC2711016  PMID: 17956854
Adaptation; aquatic plants; ethylene; flooding; growth; hypoxia; plant hormones; signal transduction; stress; submergence; review; rice

Results 1-4 (4)