Chemical root to shoot signaling under drought

doi:10.1016/j.tplants.2008.04.003

Trends in Plant Science

Volume 13, Issue 6, June 2008, Pages 281-287

https://doi.org/10.1016/j.tplants.2008.04.003 Get rights and content

Chemical signals are important for plant adaptation to water stress. As soils become dry, root-sourced signals are transported via the xylem to leaves and result in reduced water loss and decreased leaf growth. The presence of chemical signals in xylem sap is accepted, but the identity of these signals is controversial. Abscisic acid (ABA), pH, cytokinins, a precursor of ethylene, malate and other unidentified factors have all been implicated in root to shoot signaling under drought. This review describes current knowledge of, and advances in, research on chemical signals that are sent from roots under drought. The contribution of these different potential signals is discussed within the context of their role in stress signaling.

Section snippets

Chemical and hydraulic signaling under drought stress

Numerous studies have shown that plant roots can sense changes in abiotic factors such as soil water content 1, 2, soil bulk density or compaction [3], soil oxygen content [4] and changes in the nutrient composition of soil (both enrichment and depletion) [5]. Root sensing of water deficit has been widely studied, and this review focuses on the outcomes of the early stage of water-deficit sensing: the transport through the xylem of chemical signals that ultimately reduce leaf transpiration and

Agricultural practices involving chemical signals: deficit irrigation and partial root-zone drying

Root to shoot signaling under conditions of both mild and severe drought is an important area for research because of its implications for agricultural production and the WUE of plants. Fresh water supplies are predominantly used for agriculture, but this usage will need to be reduced in the future as supplies become limited. Where irrigation can be manipulated, researchers have experimented with, and successfully implemented, both deficit irrigation and partial root-zone drying (PRD) 9, 10.

ABA is a key regulator of leaf stomatal conductance

The production of ABA in roots and its transport to the leaves provides the plant with a mechanism for transmitting a chemical signal to report on the water status of the soil. This system could have evolved specifically for this purpose or the chemical signal could merely be a consequence of the increased production of ABA required to maintain root growth under water deficit [16]. A dominant role for ABA in root to shoot signaling under drought and in the control of stomatal conductance was

Involvement of pH in signaling

Changes in the pH of xylem sap commonly observed under drought stress can be an important component of root to shoot signaling and may act synergistically with ABA. In many plant species (e.g. sunflower [Helianthus annuus] [34], Phaseolus coccineus [35] and C. communis [36]), xylem sap pH becomes more alkaline when plants are water stressed and this leads to enhanced stomatal closure and even reduced growth. The potential effects of pH have been outlined previously [37] and include: i) changes

Conjugates of ABA as potential signals

Although ABA seems to play a dominant role in root to shoot signaling under drought, it also seems likely, on the basis of several studies, that other substances are also involved. ABA is present in xylem sap in conjugated forms, such as abscisic acid-glucose ester (ABA-GE). It has been suggested that a conjugated form of ABA could serve as a transported form of the hormone and, moreover, as a stress signal 32, 54. As many as six ABA conjugates have been found in xylem sap from well-watered and

Cytokinins as signals

Cytokinins could also be an important signal traveling from roots to the shoots. Root-produced cytokinins are clearly involved in responses to nutrient deprivation [5] and, as they are produced mainly in roots, could be important in drought responses [58]. Despite this, there have been few reports that provide information on the cytokinin content of xylem sap and how that content changes under drought conditions. In grapevines, a 50% reduction in zeatin (Z) and zeatin riboside (ZR) was found in

Other chemical signals

Chemical and protein-based factors other than ABA, cytokinins or pH could also be involved in root to shoot signaling. Although it has now been established clearly that xylem sap from many plant species contains proteins 66, 67, the presence of peptides in xylem sap has only recently been demonstrated [68]. The addition of xylem sap from tomato induced rapid alkalinization in a tomato cell-suspension bioassay within minutes. This approach has been used previously to identify peptides. In an

Conclusions

The production of root-sourced chemical signals under conditions of water deficit has been associated with reduced transpiration and/or leaf growth. However, the identity and relative contribution to signaling of these root-sourced chemicals remains controversial. This controversy may be due to differing responses between species, the different intensities of stress treatments applied, the time at which samples were collected during the imposition of drought, and/or the different methods used

Acknowledgements

DPS was supported in part by NSF-Plant Genome #0211842. JQDG is the recipient of an Australian Research Council Post-doctoral Fellowship (Inductry linkage project #LP0775362)

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Trends in Plant Science

ReviewChemical root to shoot signaling under drought

Section snippets

Chemical and hydraulic signaling under drought stress

Agricultural practices involving chemical signals: deficit irrigation and partial root-zone drying

ABA is a key regulator of leaf stomatal conductance

Involvement of pH in signaling

Conjugates of ABA as potential signals

Cytokinins as signals

Other chemical signals

Conclusions

Acknowledgements

Agric. Water Manag.

Field Crops Res.

Plant Sci.

Trends Plant Sci.

Trends Plant Sci.

Biochem. Biophys. Res. Commun.

Trends Plant Sci.

Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture

New Phytol.

ABA-based chemical signalling: the co-ordination of responses to stress in plants

Plant Cell Environ.

Effects of soil strength on the relation of water-use efficiency and growth to carbon isotope discrimination in wheat seedlings

Plant Physiol.

Regulation of K+ uptake and transport to the xylem in barley roots; K+ distribution determined by electron probe X-ray microanalysis of frozen-hydrated cells

J. Exp. Bot.

Nutrient sensing and signaling: NPKS

Annu. Rev. Plant Biol.

Soil water status affects the stomatal conductance of fully turgid wheat and sunflower leaves

Aust. J. Plant Physiol.

Relationships between xylem sap constituents and leaf conductance of well-watered and water-stressed maize across three xylem sap sampling techniques

J. Exp. Bot.

A hydraulic signal in root-to-shoot signalling of water shortage

Plant J.

Deficit irrigation for reducing agricultural water use

J. Exp. Bot.

Partial rootzone drying: effects on growth and fruit quality of field-grown grapevines (Vitis vinifera)

Funct. Plant Biol.

Soil moisture heterogeneity during deficit irrigation alters root-to-shoot signaling of abscisic acid

Funct. Plant Biol.

Grapevine shoot growth and stomatal conductance are reduced when part of the root system is dried

Vitis

Regulation of leaf and fruit growth in plants growing in drying soil: exploitation of the plants’ chemical signaling system and hydraulic architecture to increase the efficiency of water use in agriculture

J. Exp. Bot.

Confirmation that abscisic-acid accumulation is required for maize primary root elongation at low water potentials

J. Exp. Bot.

Root signals and the regulation of growth and development of plants in drying soil

Annu. Rev. Plant Physiol. Mol. Biol.

A leaf elongation assay detects an unknown growth inhibitor in xylem sap from wheat and barley

Aust. J. Plant Physiol.

Antitranspirant activity in xylem sap of maize plants

J. Exp. Bot.

Guard cell signal transduction

Annu. Rev. Plant Physiol. Mol. Biol.

Characterization of a wilty sunflower (Helianthus annuus L.) mutant III. Phenotypic interaction in reciprocal grafts from wilty mutant and wild-type plants

J. Exp. Bot.

Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying

J. Exp. Bot.

Growth and water relations of wilty mutants of tomato (Lycopersicon esculentum Mill.)

J. Exp. Bot.

Does engineering abscisic acid biosynthesis in Nicotiana plumbaginifolia modify stomatal response to drought?

Plant Cell Environ.

Regulation and manipulation of ABA biosynthesis in roots

Plant Cell Environ.

Abscisic acid produced in dehydrating roots may enable the plant to measure the water status of the soil

Plant Cell Environ.

How do roots control xylem sap ABA concentration in response to soil drying

Plant Cell Physiol.

Relative contribution of apices and mature tissues to ABA synthesis in droughted maize root systems

Plant Cell Physiol.

Increased synthesis of ABA in partially dehydrated root tips and ABA transport from roots to leaves

J. Exp. Bot.

Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering

Plant Growth Regul.

Abscisic acid is not the only stomatal inhibitor in the transpiration stream of wheat plants

Plant Physiol.

Scion photosynthesis and leaf gas exchange in Vitis vinifera L. cv. Shiraz: Mediation of rootstock effects via xylem sap ABA

Aust. J. Grape Wine Res.

Stomatal response to drying soil in relation to changes in the xylem sap composition of Helianthus annus. I. The concentration of cations, anions, amino acids in, and pH of, the xylem sap

Review
Chemical root to shoot signaling under drought

Regulation of K⁺ uptake and transport to the xylem in barley roots; K⁺ distribution determined by electron probe X-ray microanalysis of frozen-hydrated cells