responses to drought and phosphorus deficiency-and phytohormone

2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1436-8730/05/0408-531

J. Plant Nutr. Soil Sci. 2005, 168, 531–540 DOI: 10.1002/jpln.200520507 531

Plant responses to drought and phosphorus deficiency: contribution ofphytohormones in root-related processesLutz Wittenmayer1* and Wolfgang Merbach1

1 Martin-Luther-Universität Halle-Wittenberg, Landwirtschaftliche Fakultät, Institut für Bodenkunde und Pflanzenernährung,Adam-Kuckhoff-Straße 17b, D-06108 Halle (Saale), Germany

Accepted June 11, 2005 PNSS P05/07P

Summary—ZusammenfassungEnvironmental stresses are one of the most limiting factors inagricultural productivity. A large portion of the annual cropyield is lost to pathogens (biotic stress) or the detrimentaleffects of abiotic-stress conditions. There are numerousreports about chemical characterization of quantitatively sig-nificant substrate fluxes in plant responses to stress factorsin the root-rhizosphere system, e.g., nutrient mobilization,heavy-metal and aluminum immobilization, or establishmentof plant-growth-promoting rhizobacteria (PGPR) by exudationof organic anions, phytosiderophores, or carbohydrates intothe soil, respectively. The hormonal regulation of theseresponses is not well understood. This paper highlights thiscomplex process, stressing the involvement of phytohor-mones in plant responses to drought and phosphorus defi-ciency as examples. Beside ethylene, abscisic acid (ABA)plays an important role in drought-stress adaptation of plants.This hormone causes morphological and chemical changesin plants, ensuring plant survival under water-limited condi-tions. For example, ABA induces stomata closure, reductionin leaf surface, and increase in root : shoot ratio and, thus,reduction in transpiration and increase in soil volume forwater uptake. Furthermore, it supports water uptake in soilwith decreasing water potential by osmotic adjustment. Suit-ability of hormonal parameters in the selection for improvingstress resistance is discussed. Auxins, ethylene, and cytoki-nins are involved in morphological adaption processes tophosphorus (P) deficiency (increase in root surface, e.g., bythe formation of more dense root hairs or cluster roots).Furthermore, indole-3-acetic acid increases root exudationfor direct and indirect phosphorus mobilization in soil. Never-theless, the direct use of the trait “hormone content” of a par-ticular plant organ or tissue, for example the use of thedrought-stress-induced ABA content of detached leaves inplant breeding for drought-stress-resistant crops, seems tobe questionable, because this procedure does not considerthe systemic principle of hormonal regulation in plants.

Key words: phytohormones / drought stress / phosphorus deficiency /rhizosphere / root

Reaktionen von Pflanzen auf Trockenstress undPhosphormangel: Die Rolle von Phytohormonen inwurzelbezogenen ProzessenUmweltstress stellt den wesentlichsten Limitierungsfaktor fürdie landwirtschaftliche Produktion dar. Ein erheblicher Teilder jährlichen Ernten geht durch pathogene Organismen (bio-tischer Stress) oder durch die verheerende Wirkung abioti-scher Stressoren verloren (v. a. Trockenstress und Nährstoff-mangel). Es gibt zahlreiche Untersuchungen zur stofflichenCharakterisierung der pflanzlichen Stressreaktion an derWurzel, z. B. Nährstoffmobilisierung, Schadstoffimmobilisie-rung oder Etablierung von wachstumsfördernden Rhizobak-terien durch Wurzelabscheidungen. Die hormonelle Steue-rung dieser Prozesse ist bisher weniger erforscht. Der Artikelgeht dieser Problematik am Beispiel von Trockenstress undPhosphormangel unter besonderer Berücksichtigung vonPhytohormonen nach. Bei der Anpassung von Pflanzen anWassermangelbedingungen spielt neben Ethylen das Phyto-hormon Abscisinsäure (ABA) eine wichtige Rolle. Es induziertmorphologische und chemische Veränderungen in derPflanze, die ein Überleben unter Wassermangelbedingungenermöglichen. Beispielsweise induziert die ABA den Stomata-schluss, eine Verringerung der Blattoberfläche sowie eineErhöhung des Wurzel:Spross-Verhältnisses und bewirktdadurch eine verringerte Transpiration und Vergrößerung desBodenvolumens zur Erschließung von Wasservorräten. Da-rüber hinaus kann eine ABA-induzierte Anreicherung vonosmotisch wirksamen Verbindungen zur Wasseraufnahmebei sinkendem Wasserpotential im Boden beitragen. BeiPhosphat (P)-Mangel sind vor allem Auxine, Cytokine undEthylen an der morphologischen Anpassung der Wurzeln(Vergrößerung der Wurzeloberfläche durch verstärkte Bil-dung von Wurzelhaaren oder Proteoidwurzeln) beteiligt. Da-rüber hinaus bewirkt Indolyl-3-Essigäure eine Intensivierungder Abgabe von Wurzelabscheidungen zur direkten oder indi-rekten P-Mobilisierung in der Rhizosphäre. Trotzdem wird dieunmittelbare Verwendung des Indikators „Hormongehalt“eines bestimmten Pflanzenorganes, beispielsweise dertrockenstressinduzierte ABA-Gehalt von abgeschnittenenBlättern, für die Züchtung auf Stressresistenz als problema-tisch angesehen, da sie das systemische Prinzip der Hor-monregulation nicht berücksichtigt.

1 Introduction

Knowledge about plant responses to various stress factorsand the relationship between suboptimal environmental con-ditions and plant growth and crop yield is very important forseveral reasons: First, land areas affected by various stress

factors have to be used in agricultural production at present.Furthermore, regions with partially very low suitability for agri-cultural use (e.g., marginal soils, zones with water limitation)are the only way for expansion of field areas and, thus, forincreasing food production necessary for a growing worldpopulation (European Parliament, 1999; Smithson andSanchez, 2001; Williams, 2002). Second, climatic changes(e.g., long-term increase in temperature with simultaneousdecrease in precipitation in central and eastern Germany)

* Correspondence: Dr. L. Wittenmayer;e-mail [email protected]

may result in more frequent stress events even in regionstraditionally used for agricultural purposes (BMBF, 2003;Gerstengarbe et al., 2003; Hulme and Sheard, 1999; Umwelt-bundesamt, 2002).

In Africa, South Asia, and Australia, half of the total landareas are affected by water deficiency, while in South Amer-ica and Southeast Asia, mineral imbalances are the dominat-ing factors. Thus, drought and chemical constrains are themajor limitations to agricultural use of land (Smithson andSanchez, 2001). After nitrogen (N), P is usually the most lim-iting nutrient for crop production (Schachtman et al., 1998).Therefore, due to their importance in agricultural production,drought and P deficiency are illustrated here in more detail.

Plants develop a wide range of strategies to cope with stresssituations. Under conditions of water deficiency, droughtescape and drought tolerance are two important strategies toensure plant growth (Bänziger et al., 2000). In the first case,plants finish their growth period before drought stress mayaffect yield formation. In plant breeding, this strategy is con-sidered by selection for earliness. Drought tolerance may beincreased by morphological or chemical changes of plants,e.g., stomatal regulation (Wilkinson and Davies, 2002),reduction of the plant surface, increased root : shoot ratio,accumulation of osmolytes (Chen and Murata, 2002; Nayyarand Walia, 2004), or rhizosphere processes (McCully andBoyer, 1997). For example, Walker et al. (2003) speculatedthat root exudates could play a major role in the maintenanceof root-soil contact, which is especially important to the plantunder drought and drying conditions, when hydraulic continu-ity will be lost. Young (1995) found that rhizosheath soil wassignificantly wetter than bulk soil and suggested that exu-dates within the rhizosheath increase the waterholding capa-city of the soil.

Under P-stress conditions, strategies for improving phos-phorus-use efficiency are: first, increasing the root surface-soil contact area by modifying root morphology; second,increasing the effective root area by root symbiosis witharbuscular mycorrhizal fungi; and third, increasing nutrientavailability through rhizosphere modification (e.g., shiftingpH, release of reductans or chelators) (Hinsinger et al., 2003;Jones et al., 2004; Randall et al., 2001; Rubio et al., 2003;Ryan et al., 2001; Schilling et al., 1998; Vance et al., 2003).The use of these traits in plant breeding, particularly the im-provement of root morphology, is time-consuming and labor-intensive and, therefore, limits its application in breeding pro-grams where large numbers of genotypes need to bescreened (Ortiz-Monasterio et al., 2001; Sinclair and Vadez,2002). Due to their better accessibility, shoot-related para-meters were mostly considered in the selection processes inpast decades. There is much less information about rootcharacteristics important for stress resistance. Particularlythe regulation of stress responses in the root-rhizospheresystem is not well understood. Doubtless, phytohormonesplay an essential role in these processes (Casson andLindsey, 2003; Forde and Lorenzo, 2001; Weyers and Pater-son, 2001). It is frequently observed that the plant’sresponses to drought or P deficiency can be mimicked byexogenously applying a particular plant hormone, though hor-

monal involvement in mineral-stress adaptation is discussedcontroversially (Forde and Lorenzo, 2001). But even whenthe root was the stressed organ, hormonal changes havebeen mostly measured in shoot or xylem sap (Henson, 1984;Itai, 1999; Kozlowski and Pallardy, 2002; Tuberosa et al.,1992; Zhang and Davies, 1987). Therefore, the contributionof hormones to drought and phosphorus-deficiency respon-ses of roots was reviewed here.

2 Drought stress

While accumulation of osmolytes like proline or sugars isinduced by severe drought stress, slight changes in plantwater potential may result in a substantial increase in ABAcontent, making this compound a very sensitive drought-stress indicator (Hartung, 1996). The root is a significantsource for ABA in intact plants (Wilkinson and Davies, 2002;Zhang and Davies, 1987). Its biosynthesis in roots and trans-port via the xylem to the shoot may induce drought-stress-adaptation responses in aboveground organs before sub-stantial changes in shoot water potential are detectable.Although it is known that carotenoid precursors of ABA areproduced in plastids and the final steps of ABA biosynthesisare believed to be cytosolic, the precise locations of biosyn-thetic enzymes and translocation pathways of various inter-mediates have not been determined (Seo and Koshiba,2002). Two pathways have been proposed for the synthesisof ABA (Milborrow, 2001). In the “direct pathway”, which hasbeen shown to operate in some fungi, ABA is derived fromfarnesyl diphosphate (Hirai et al., 2000). Because of struc-tural similarities, an “indirect pathway”, in which ABA isproduced from the cleavage of carotenoids, also has beenproposed (Taylor and Smith, 1967). The latter is supported byexperiments with mutant plants investigating genes andenzymatic activities (Cheng et al., 2002; González-Guzmánet al., 2002; Schwartz et al., 2003).

Over the last decade, much attention has been paid to ABAconjugates in the xylem sap of various plants (Sauter et al.,2002). Munns and King (1988) and Munns et al. (1993)reported that an unidentified ABA conjugate is more impor-tant as a long-distance stress signal than free ABA. After arri-val in the leaf tissue, this complex form is believed to be phy-siologically more active than ABA. Bano et al. (1993, 1994)were the first to identify ABA glucose ester (ABA-GE) in thexylem sap of rice and sunflower plants. According to Sauterand Hartung (2000) and Sauter et al. (2002), endogenousABA conjugates are formed in the cytosol of root cells, trans-ported symplastically to the xylem parenchyma cells andreleased to the xylem vessels. Because of its extremelyhydrophilic properties, ABA glucose ester (ABA-GE) is trans-located in the xylem of the stem without any loss to the sur-rounding parenchyma. After arrival in the leaf apoplast, trans-porters for ABA-GE in the plasmalemma have to be postu-lated to redistribute the conjugates to the mesophyll cells.Additionally, apoplastic esterases can cleave the conjugateand release free ABA to the target cells and tissues. Theactivity of these esterases is increased when barley plantsare subjected to salt stress. Wittenmayer and Schilling (1998)observed a simultaneous drought-stress-induced increase infree- and conjugated-ABA content of sugar-beet leaves of

2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

532 Wittenmayer, Merbach J. Plant Nutr. Soil Sci. 2005, 168, 531–540

intact plants, though sugar-beet tap roots seemingly fail toproduce ABA (Schulte-Altedorneburg et al., 1989).

Experiments with the application of free ABA to well-wateredplants support its role in drought-stress adaptation (Xu et al.,2002). The addition of ABA (0.1 mmol L–1) to the nutrientsolution decreased the average leaf number, area of fullydeveloped leaf and the dry weight per plant of six Trifoliumsubterraneum L. cultivars by 50%, whereas root : shoot ratiowas increased by 80%. In sugar-beet plants (Beta vulgarisssp. vulgaris var. altissima Döll), moderate drought stressand application of a nutrient solution containing 0.1 mmol L–1

ABA to well-watered sugar-beet plants resulted in similargrowth responses: reduction of leaf area by 40% andincrease of root : shoot ratio by about 38% (Wittenmayer,2001; Wittenmayer et al., 2004). In this particular crop plant,an ABA-induced increase in root : shoot ratio correlates withthe harvest index (HI) and may contribute to a higher or morestable yield performance under drought stress. In other crops(i.e., where the root does not contribute to the HI), increasedABA content may result in lower yields (Blum et al., 1997).

Saab et al. (1990) observed that ABA is necessary for main-taining root growth in drying soil. Later, it has been reportedthat ABA plays a role in promoting root growth independentof its effects on plant water balance (Sharp et al., 2000; Spol-len et al., 2000). It was suggested (Cheng et al., 2002; Wit-tenmayer, 1992) that ABA may possess dual functions: as agrowth inhibitor in the presence of severe drought stress(characterized by induced high endogenous ABA content)and a promoter of root growth in the absence of stress orunder moderate-stress conditions (associated with relativelylow endogenous ABA levels). Alternatively, ABA could func-tion as a growth inhibitor in certain cells, tissues, or organs(e.g., shoot) and as growth promoter in other organs (e.g.,roots). The ability of ABA to act as either a promoter or aninhibitor of downstream processes likely depends on thedownstream signaling components, such as transcription fac-tors, that may operate in tissue, development, and/or on theinteractions of ABA with other hormones, such as ethylene(Eckardt, 2002; Sharp, 2002; Sharp and LeNoble, 2002). Forexample, studies in maize (Spollen et al., 2000) suggest thatthe stunted growth of ABA-deficient plants is caused by theoverproduction of ethylene and that one function of ABA maybe to prevent the overproduction of ethylene. Recent resultsindicate a participation in the regulation of aquaporins (Luuand Maurel, 2005).

Abscisic acid affects also the accumulation and transport ofosmotically active molecules and ions (e.g., proline, glycinebetaine, Na+, K+, Ca2+, and Cl–) and, thus, the nutritional sta-tus of the plant (Chen and Murata, 2002; Younis et al., 1994).Younis et al. (1994) observed that the addition of ABA at aconcentration of 1 mmol L–1 increased proline and phos-phorus concentration in Phaseolus vulgaris L. Furthermore,abscisic acid stimulates the transport of K+, Ca2+, and Cl–

from root to shoot and accumulation of K+, Na+, and Cl– inroot cells and inhibits the transport of Na+ and accumulationof Ca2+. It also affects nitrate reductase activity in Cichoriumintybus L. (Goupil et al., 1998).

Occurrence of ABA is not restricted to plant tissues. The hor-mone occurs also in the rhizosphere and in soil after beingexuded by plant roots or originated by microorganisms (Hallet al., 1986; Hartung et al., 1996; Müller et al., 1989; Rivier etal., 1983; Slovik et al., 1995). Degenhardt et al. (2000) foundthat in alkaline soil substrates, considerable portions of theABA synthesized in the roots leached out into the soil solutionof the rhizosphere. Passioura (2002) speculates that the roottips may continually produce a low level of inhibitor, which infavorable soil conditions, but not in unfavorable, disperses bydiffusing into the neighboring soil. If soil dryness or poor con-tact with the soil (loose soil or roots in biopores) inhibits suchdispersion, this putative inhibitor could build up in concentra-tion within the tip and eventually find its way into the tran-spiration stream and thence to the leaves.

3 Phosphorus deficiency

Plants have evolved sophisticated metabolic and develop-mental strategies to conserve inorganic phosphate (Pi) and tomaximize its acquisition from the rhizosphere when Pi is limit-ing (Ticconi et al., 2004). Examples for biochemical adapta-tions include bypass reactions of adenylate- and Pi-depen-dent steps in respiratory pathways (Plaxton and Carswell,1999), enhanced expression of high-affinity Pi transporters(Raghothama, 1999) and changes of membrane-lipid compo-sition (Härtel and Benning, 2000; Yu et al., 2002) and ofsugars/photosynthates as crucial components in P-deficiencysignal transduction (Liu et al., 2005; Müller et al., 2005).Remodeling of root-system architecture and increased root-hair formation affecting surface, density, and length of rootsto accelerate soil exploration are typical developmentalresponses to low Pi, because of low P mobility in soil (López-Bucio et al., 2003; Ma et al., 2001; Williamson et al., 2001).Furthermore, an increased assimilate allocation to rootsresults in a higher root : shoot ratio (Fredeen et al., 1989; Yanet al., 1996). Lynch and Brown (2001) report that root sys-tems with enhanced topsoil foraging acquire phosphorusmore efficiently than others of equivalent size. Comparisonsof contrasting genotypes in controlled environments and inthe field show that plants with better topsoil foraging havesuperior phosphorus acquisition and growth in low-phos-phorus soils. It appears that many architectural responses tophosphorus stress may be mediated by plant hormones (deGroot et al., 2003; Ma et al., 2003). Genetic mapping of thesetraits shows that they are quantitatively inherited, but can betagged with QTLs that can be used in plant-breeding pro-grams (Lynch and Brown, 2001). New crop genotypes incor-porating these traits have substantially improved yield in lowphosphorus soils, and are being deployed in Africa and LatinAmerica (CIAT, 1999; Ortiz-Monasterio et al., 2001). Despitenumerous physiological studies on adaptation responses to Pstarvation, little is known about the underlying hormonal pro-cesses. Table 1 shows the effect of plant growth regulatortreatment applied with nutrient solution on the root surface ofmaize depending on P availability. In untreated control plants,phosphorus deficiency (–P) increased the root surface by17%. The addition of indole-3-acetic acid (IAA), gibberellicacid (GA3), and trans-zeatin (t-Z) to the nutrient solution of–P plants increased the root surface by 31%, 44%, and 49%,respectively. Thus, the tested hormones may increase the


J. Plant Nutr. Soil Sci. 2005, 168, 531–540 Plant responses to drought and phosphorus deficiency 533

root surface and, thus, mimic P-deficiency behavior of theplant. Furthermore, +P and –P plants responded differently tohormone application, indicating a varying responsiveness tohormones depending on the nutrition status of the plant.

Particularly root hairs contribute to phosphorus acquisition byextending the zone of phosphorus depletion around roots(Föhse et al., 1991). Auxins, ethylene, and cytokinins act atseveral stages of their formation (Bibikova and Gilroy, 2002;Ma et al., 2003; Romera and Alcantara, 2004; Schikora andSchmidt, 2002). Auxin treatment of the root-hairless ricemutant “RH2” induced very short root hairs, suggesting thatthe absence of root hairs in “RH2” may be due to a shortageof endogenous auxin (Suzuki et al., 2003).

The control of plant responses do P deficiency by endogen-ous phytohormones may be affected by microbial hormoneproduction in the rhizosphere. Studies utilizing indole-3-aceticacid (IAA)-producing PGPR and Arabidopsis that contain anauxin-responsive GUS fusion suggest that plants perceiveIAA released by bacteria in the rhizosphere (O’Callaghan etal., 2001). The hormonal interaction between plant andmicrobia is not limited to auxin-producing bacteria (Biswas etal., 2000; Höflich and Kühn, 1996; Marschner et al., 1986).There are several reports about the correlation between thecapability of microbial gibberellin (Gutiérraz-Mañero et al.,2001) and cytokinin biosynthesis and the plant-growth-pro-moting effect of inoculated rhizobacteria. López-Bucio et al.(2002) found that at P-limiting conditions (50 lmol L–1), theArabidopsis root system undergoes major architecturalchanges in terms of lateral-root number, lateral-root density,and primary-root length. Treatment with auxins and auxinantagonists indicate that these changes are related to anincrease in auxin sensitivity in the roots of P-deprived Arabi-dopsis seedlings.

Neumann et al. (2000) observed increased formation of clus-ter roots in white lupin (Lupinus albus L.) when indole aceticacid was supplied to the growth medium of P-sufficientplants, whereas cluster-root formation was inhibited by kine-tin application. This suggests the involvement of endogenousphytohormones (auxins and cytokinins), which may act in anantagonistic manner in the P-starvation response. Lamont(2003) reports that root-cluster production is controlled by theinterplay between external and internal nutrient levels, andmediated by auxin and other hormones to which the processis particularly sensitive. Interestingly, cluster roots induced byauxin application do not show increased phosphoenolpyruva-

tecarboxylase (PEPC) activity or root exudation, showing thatauxin alone is insufficient for the whole proteoid root re-sponse (Gilbert et al., 2000). High sugar concentrations inplant tissues increase lateral-root production, and severalhormones control root development interactively with carbo-hydrates (Laby et al., 2000). Although these findings revealedthe involvement of phytohormones in Pi-deficiency re-sponses, not much is known about their role in the Pi-starva-tion-induced signaling pathways or in gene expression. Inhi-bitors of auxin transport and ethylene synthesis have beenshown to influence the expression of genes during Pi defi-ciency in the proteoid roots of white lupin (Gilbert et al.,2000). A report by Martin et al. (2000) shows the suppressionof Pi-starvation-induced gene expression by cytokinins. Thecytokinin effects are presumed to be due to altered longdistance signaling during Pi starvation. Thus, there is growingevidence supporting the differential effect of hormones on Pi-starvation-induced responses (Karthikeyan et al., 2002). Thishas been clearly demonstrated in the proteoid roots of whitelupin, wherein auxin-transport inhibitors decreased the levelsof Pi-starvation-induced PEPC and malate dehydrogenase,but not the secretion of acid phosphatase (Gilbert et al.,2000). Similarly, cytokinins have been shown to suppress theexpression of some Pi-starvation-induced genes, but not themodifications of root growth (Martin et al., 2000).

Much of the reason for the continued need for P fertilization isdue to the slow conversion of P to plant-unavailable forms orP fixation in soil (Smithson and Sanchez, 2001). Sparinglysoluble P sources in the rhizosphere can be mobilizedthrough the action of root exudates, including phosphatases,organic acids, and carbohydrates (Dakora and Phillips, 2002;Jones, 1998; Nguyen, 2003). The latter, particular carbohy-drates, may serve as a carbon source for P-mobilizing micro-organisms (Harrison, 1999; Hinsinger, 2001; Hinsinger et al.,2003; Paterson, 2003). Table 2 shows the effect of P avail-ability and IAA application to roots on the sugar release bymaize roots into the rhizosphere

While the effect of IAA application to plants sufficiently sup-plied with P was negligible, treatment of P-deficient plantswith IAA increased carbohydrate release by 52%. Water-soluble carbohydrates are an important and easily availablecarbon source for P-solubilizing microorganisms.

The activity of acid phosphatase is considered to play animportant role in the mineralization of organic P in soil, and itis regarded as an indicator for P deficiency in plants (Barrett-


Table 1: Effect of P availability and hormone treatment on the size of the root surface (in dm2 per plant) of maize (cultivar “Bezemara”). +P:water-soluble P (1.3 mmol L–1); –P: sparingly soluble P (1 mmol Ca3(PO4)2 per pot); IAA: 100 lmol L–1 indole-3-acetic acid; GA3: 100 lmol L–1

gibberellic acid 3; t-Z: 10 lmol L–1 trans-zeatin; means ± standard deviation, n = 4 (from Wittenmayer et al., 2003, 2004).Tabelle 1: Wirkung von P-Verfügbarkeit und Hormonbehandlung auf die Größe der Wurzeloberfläche (in dm2 pro Pflanze) bei der Maissorte„Bezemara“. +P: wasserlösliches P (1,3 mmol L–1), –P: schwerlösliches P (1 mmol Ca3(PO4)2 je Anzuchtgefäß); IAA: 100 lmol L–1 Indolyl-3-Essigsäure; GA3: 100 lmol L–1 Gibberellinsäure 3; t-Z:10 lmol L–1 trans-Zeatin; Mittelwerte ± Standardabweichung, n = 4 (aus Wittenmayer etal., 2003, 2004).

P availability Applied hormone

0 IAA GA3 t-Z+P 2.09± 0.24 2.28±0.36 2.91±0.12 2.86±0.28–P 2.45±0.13 2.75±0.28 3.03±0.21 3.12±0.24


Lennard and Greenway, 1982; McLachlan and De Marco,1982), particularly in the rhizosphere (Ascencio, 1997; Taraf-dar and Jungk, 1987). Asmar et al. (1995) found differencesin barley genotypes in their ability to induce soil phosphataseactivity. The level of induced phosphatase activity was corre-lated with the hydrolysis of organic-P compounds within theroot hair zone.

The effects of IAA treatment on acid-phosphatase activity inthe rhizosphere are shown in Tab. 2. Application of IAA to P-deficient plants increased acid-phosphatase activity 2.5 timesin comparison to untreated +P plants. However, the exactrole of phosphatase is not yet totally clear, as the majororganic-P compound in soil, inositol P and phytate can be apoor substrate for phosphatases (Clarkson, 1985). Further-more, it is unlikely that plants would successfully compete fororganic P with soil microorganisms. A possible role for phos-phatases might be to recover Pi from organic P lost from plantin the immediate vicinity of the roots (Sinclair and Valdez,2002).

4 Conclusions

The presented data highlight the possible hormonal effectson physiological stress responses to drought stress andphosphorus deficiency.

In drought stress, ABA plays an important role. The applica-tion of this PGR may induce drought-stress responses evenin well-watered plants. These results support the assumptionthat ABA accumulation and drought-stress responses arecausally related.

Davies et al. (2002) have shown how an understanding of thedrought-stress physiology of the whole plant can lead to sub-stantial savings of irrigation water in agriculture using “partialroot zone drying”. This irrigation technique has been devel-oped to allow exploitation of the plant’s long distance signal-ing system. When the system is optimized, stomatal behav-ior, shoot water status, and leaf growth can be regulated suchthat water-use efficiency (fruit yield : water used) can be sig-nificantly increased.

Due to genetic variability and heritability of drought-inducedABA accumulation, the ABA content can be used to selectdrought-resistant plants (Quarrie, 1981, 1996). There arereports about genetic modification of ABA biosynthesis(Quarrie et al., 1997; Tan et al., 1997). Though at presentplant breeders frequently fail to use the “ABA content” or the“ABA biosynthesis capacity” as a trait in selecting fordrought-stress tolerance. In some cases, genotypes thatwere selected for a high capacity for ABA accumulation underdrought stress were found to be not better or even worsethan the normal ones in terms of function and yield underdrought stress (Blum et al., 1997). Obviously, manipulation ofABA content alone is not necessarily correlated positivelywith yield performance under drought stress. Furthermore,screenings measuring the capacity to accumulate ABA indetached shoot organs (Henson, 1984) do not consider thecontribution of root-derived ABA in the stress response of theintact plant and ignore different ways in regulation of ABAcontent in plant tissue depending on dynamics of stress de-velopment (Wittenmayer and Schilling, 1998). Therefore, thisparameter is not a good indicator for drought-stress resis-tance suitable in plant breeding.

The effect and interaction of phytohormones on root re-sponse to P deficiency is more complex. It is known that IAAeffects depend on hormone doses. While low concentrationspromote root growth, high IAA amounts inhibit plant develop-ment (Teale et al., 2005). Our findings that +P and –Presponded differently to IAA application agree with resultsfrom López-Bucio et al. (2002) and support the demand fortesting and selecting plant genotypes under stress as well asunder optimal conditions. When advanced genetic materialsare evaluated only under high-input conditions, this some-times results in genotypes that are outstanding under low-Pconditions, but intermediate under high-input conditions. Thisgermplasm might be overlooked if it is tested only under high-input conditions, due to its intermediate performance underthis condition. Hence, it is important to select and evaluateunder both low- and high-nutrient conditions (Ortiz-Monas-terio et al., 2001). Though IAA application to the root wasaccompanied by higher acid-phosphatase activity in the plantrhizosphere, the effect of higher IAA content of roots or higherresponsiveness to rhizosphere auxins on other processeshave to be tested due to the systemic trait of hormone


Table 2: Effect of P availability and hormone treatment on sugar release and acid-phosphatase activity in the rhizosphere of maize (cultivar“Lenz”). +P: water-soluble P (1.3 mmol L–1); –P: sparingly soluble (1 mmol Ca3(PO4)2 per pot); IAA: 100 lmol L–1 indole-3-acetic acid; means ±standard deviation, n = 4 (Wittenmayer et al., 2004; unpublished data).Tabelle 2:: Wirkung von P-Verfügbarkeit und Hormonbehandlung auf die Zuckerabgabe und die Aktivität saurer Phosphatasen in der Rhizo-sphäre der Maissorte „Lenz“. +P: wasserlösliches P (1,3 mmol L–1), –P: schwerlösliches P (1 mmol Ca3(PO4)2 je Anzuchtgefäß); IAA: 100 lmolL–1 Indolyl-3-Essigsäure; Mittelwerte ± Standardabweichung, n = 4 (Wittenmayer et al., 2004; unveröffentlicht).

Rhizosphere parameter P availablity Hormone treatment

0 IAA

Released sugars +P 38.6±13.0 35.9±15.7

(in nmole per plant) –P 37.9±6.9 59.4±19.0

Activity of acid phosphatases +P 11.9±2.4 15.0±9.7

(in nmol s–1 (mg protein)–1) –P 12.9±4.2 29.3±4.1


actions. Roots are capable of synthesizing all phytohormonesand, thus, the involvement of only one PGR in the regulationof an adaptation to an environmental process is questionable(Itai and Birnbaum, 1996; Passioura, 2002). Determining thelevel and the effect of one hormone may yield informationwith limited value. A reasonable solution would be systemanalysis (Trewavas, 1986) with the simultaneous determina-tion of all known PGR.

The phytohormonal regulation of the plant may be also sup-ported by hormone-producing plant-growth-promoting rhizo-bacteria (PGPR), which are screened for improving growthand yield of agricultural crops (Khalid et al., 2004; Persello-Cartieaux et al., 2003; Sahin et al., 2004; Vessey, 2003). Foran effective use of PGPR, the varying responsiveness ofcrop plants under stress and optimal growth conditionstoward microbial signaling compounds from the rhizosphereshould be considered in screening tests.

Another point which needs investigating is the molecularbasis of the action of the hormones (Bartels and Souer, 2004;Itai and Birnbaum, 1996). Using knowledge about the geneticcontrol of mineral-stress tolerance (Cianzio, 1999; Graham etal., 1992; Grover and Chandramouli, 2002; Ishikawa et al.,2002), recent methods in gene technology open fundamen-tally new avenues in stress research. By using molecular-bio-logical tools, the findings can be utilized in creating resistantplants (Bruce et al., 2002; Grover and Chandramouli, 2002;López-Bucio et al., 2000). The molecular-genetic manipula-tion of key steps in stress response and their potential use astools for improving plant nutrition, e.g., phosphate-transpor-ter-gene promoters (Rengel, 2002; Schünmann et al., 2003;Uhde-Stone et al., 2003), alteration of citrate synthesis forroot exudation (de la Fuente et al., 1997), or extracellularphytase activity (George et al., 2004, 2005) is a more promis-ing option than the manipulation of phytohormonal balancesof plants due to the complex involvement of PGR in manyother processes. The authors stressed the potential of trans-genic plants to enhance the P nutrition of crop plants and toimprove the efficiency of P-fertilizer use in agricultural sys-tems. The ecological risks of transgenic plants have to beassessed before their use (Godfree et al., 2004).

Thus, knowledge of stress-adaptation mechanisms benefitsagricultural production. If new stress-resistant cultivarsshould be selected for land areas affected by environmentalstresses, it is important to understand physiological and bio-chemical principles of plant responses to particular stresssituations. This knowledge will then allow plant breeders todefine the selection criteria for the creation of resistant crops.More than twenty years ago, Swindale and Bidinger (1981)suggested that the integration of physiological and biochem-ical parameters of stress adjustment will at least theoreticallyaccelerate the selection process and increase its efficiency incomparison to the use of yield and its stability as integralselection criteria. At present, time-consuming and laboriousmethods for direct detection of hormones and other metabo-lites by expensive analytical equipment is being replaced bymolecular-biological tools for genetic and phytohormonalcontrol mechanisms (e.g., QTL mapping; “proteomics” and“genomics”; Grover and Chandramouli, 2002; Yan et al.,

2004) usually available in plant-breeder’s laboratories.Nevertheless, phytohormonal research will be necessary inorder to find and prove the stress-adaptation mechanisms ofplants.

Acknowledgments

The authors wish to thank G. C. Calderone for correcting andimproving the English text. C. Engels and two anonymousreviewers provided very useful comments on the manuscript.

References

Ascencio, J. (1997): Root secreted acid phosphatase kinetics as aphysiological marker for phosphorus deficiency. J. Plant Nutr. 20,9–26.

Asmar, F., Gahoonia, T. S., Nielsen, N. E. (1995): Barley genotypesdiffer in activity of soluble extracellular phosphatase and depletionof organic phosphorus in rhizosphere soil. Plant Soil 172, 117–122.

Bano, A., Dörffling, K., Bettin, D., Hahn, H. (1993): Abscisic acid andcytokinins as possible root-to-shoot signals in xylem sap of riceplants in drying soil. Aust. J. Plant Physiol. 20, 109–115.

Bano, A., Hansen, H., Dörffling, K., Hahn, H. (1994): Changes in thecontent of free and conjugated abscisic acid, phaseic acid andcytokinins in the xylem sap of drought stressed sunflower plants.Phytochemistry 37, 345–347.

Bänziger, M., Edmeades, G. O., Beck, D., Bellon, M. (2000):Breeding for Drought and Nitrogen Stress Tolerance in Maize.From Theory to Practice. CIMMYT, Mexico, D. F.

Barrett-Lennard, E. G., Greenway, H. (1982): Partial separation andcharacterization of soluble phosphatases from leaves of wheatgrown under phosphorus deficiency and water deficit. J. Exp. Bot.33, 694–704.

Bartels, D., Souer, E. (2004): Molecular responses of higher plants todehydration, in Hirt, H., Shinozaki, K. (eds.): Plant Responses toAbiotic Stress. Springer Verlag, Berlin, Heidelberg, New York,Hong Kong, London, Milan, Paris, Tokyo, pp. 9–38.

Bibikova, T., Gilroy, S. (2002): Root hair development. J. PlantGrowth Regul. 21, 383–415.

Biswas, J. C., Ladha, J. K., Dazzo, F. B. (2000): Rhizobia inoculationimproves nutrient uptake and growth of lowland rice. Soil Sci. Soc.Amer. J. 64, 1644–1650.

Blum, A., Sullivan, C. Y., Nguyen, H. T. (1997): The effect of plantsize on wheat response to agents of drought stress: II. Waterdeficit, heat and ABA. Aust. J. Plant Physiol. 24, 43–48.

BMBF (2003): Herausforderung Klimawandel. Bundesministerium fürBildung und Forschung (BMBF), Berlin, www.bmbf.bund.de/pub/klimawandel.pdf

Bruce, W. B., Edmeades, G. O., Barker, T. C. (2002): Molecular andphysiological approaches to maize improvement for drought.J. Exp. Bot. 53, 13–25.

Casson, S. A., Lindsey, K. (2003): Genes and signalling in root de-velopment. New Phytol. 158, 11–38.

Chen, T. H. H., Murata, N. (2002): Enhancement of tolerance ofabiotic stress by metabolic engineering of betaines and othercompatible solutes. Curr. Opin. Plant Biol. 5, 250–257.

Cheng, W.-H., Endo, A., Zhou, L., Penney, J., Chen, H.-C., Arroyo,A., Leon, P., Nambara, E., Asami, T., Seo, M., Koshiba, M., Sheen,J. (2002): A unique short-chain dehydrogenase/reductase in Arabi-dopsis glucose signaling and abscisic acid biosynthesis and func-tions. Plant Cell 14, 2723–2743.



Cianzio, S. R. (1999): Breeding crops for improved nutrient efficiency:soybean and wheat as case studies, in Rengel, Z. (ed.): MineralNutrition of Crops: Fundamental Mechanisms and Implications.The Haword Press, New York, pp. 267–287.

CIAT (1999): Bean project 1998 annual report. Working documentnumber 179. CIAT, Cali, Colombia.

Clarkson, D. T. (1985): Factors affecting mineral nutrient acquisitionby plants. Annu. Rev. Plant Physiol. 36, 77–115.

Dakora, F. D., Phillips, D. A. (2002): Root exudates as mediators ofmineral acquisition in low-nutrient environments. Plant Soil 245,35–47.

Davies, W. J., Wilkinson, S., Loveys, B. (2002): Stomatal control bychemical signalling and the exploitation of this mechanism toincrease water use efficiency in agriculture. New Phytol. 153,449–460.

Degenhardt, B., Gimmler, H., Hose, E., Hartung, W. (2000): Effect ofalkaline and saline substrates on ABA contents, distribution andtransport in plant roots. Plant Soil 225, 83–94.

Eckardt, N. A. (2002): Abscisic acid biosynthesis gene underscoresthe complexity of sugar, stress, and hormone interactions. PlantCell 14, 2645–2649.

European Parliament (ed.) (1999): Consequences of ClimateChange for Agricultural Production. Scientific Technology Op-tions Assessment (STOA) Study No EP/IV/B/STOA/98/02/01,www.europarl.eu.int/stoa/publi/98-02-01/default_en.htm

Föhse, D., Claassen, N., Jungk, A. (1991): Phosphorus efficiency ofplants. II. Significance of rood radius, root hairs and cation-anionbalance for phosphorus influx in seven plant species. Plant Soil132, 261–272.

Forde, B., Lorenzo, H. (2001): The nutritional control of root develop-ment. Plant Soil 232, 51–68.

Fredeen, A. L., Rao, I. M., Terry, N. (1989): Influence of phosphorusnutrition on growth and carbon partitioning in Glycine max (L.)Merr. Plant Physiol 89, 225–230.

de la Fuente, J. M., Ramirez-Rodriguez, V., Cabrera-Ponce, J. L.,Herrera-Estrella, L. (1997): Aluminum tolerance in transgenicplants by alteration of citrate synthesis. Science 276, 1566–1568.

George, T. S., Richardson, A. E., Hadobas, P. A., Simpson, R. J.(2004): Characterization of transgenic Trifolium subterraneum L.which expresses phyA and releases extracellular phytase: growthand P nutrition in laboratory media and soil. Plant Cell Environ. 27,1351–1361.

George, T. S., Simpson, R. J., Hadobas, P. A., Richardson, A. E.(2005): Expression of a fungal phytase gene in Nicotiana tabacumimproves phosphorus nutrition of plants grown in amended soils.Plant Biotechnol. J. 3, 129–140.

Gerstengarbe, F.-W., Badeck, F., Hattermann, F., Krysanova, V.,Lahmer, W., Lasch, P., Stock, M., Suckow, F., Wechsung, F.,Werner, P. C. (2003): Studie zur klimatischen Entwicklung im LandBrandenburg bis 2055 und deren Auswirkungen auf den Wasser-haushalt, die Forst- und Landwirtschaft sowie die Ableitung ersterPerspektiven. PIK-Report, No. 83, Potsdam Institute for ClimateImpact Research, Potsdam.

Gilbert, G. A., Knight, J. D., Vance, C. P., Allan, D. L. (2000): Proteoidroot development of phosphorus-deficient lupin is mimicked byauxin and phosphonate. Ann. Bot. 85, 921–928.

Godfree, R. C., Young, A. G., Lonsdale, W. M., Woods, M. J.,Burdon, J. J. (2004): Ecological risk assessment of transgenicpasture plants: a community gradient modelling approach. Ecol.Lett. 7, 1077–1089.

González-Guzmán, M., Apostolova, N., Bellés, J. M., Barrero, J. M.,Piqueras, P., Ponce, M. R., Micol, J. L., Serrano, R., Rodríguez, P.

L. (2002): The short-chain alcohol dehydrogenase ABA2 catalyzesthe conversion of xanthoxin to abscisic aldehyde. Plant Cell 14,1833–1846.

Goupil, P., Loncle, D., Druart, N., Belletre, A., Rambour, S. (1998):Influence of ABA on nitrate reductase activity and carbohydratemetabolism in chicory roots (Cichorium intybus L.). J. Exp. Bot. 49,1855–1862.

Graham, R. D., Ascher, J. S., Hynes, S. C. (1992): Selecting zinc-effi-cient cereal genotypes for soils and low zinc status. Plant Soil 146,241–250.

de Groot, C. C., Marcelis, L. F. M., van den Boogaard, R., Kaiser, W.M., Lambers, H. (2003): Interaction of nitrogen and phosphorusnutrition in determining growth. Plant Soil 248, 257–268.

Grover, A., Chandramouli, A. (2002): Abiotic stress tolerant trans-genics in the days of genomics and proteomics. Physiol. Mol. Biol.Plants 8, 193–211.

Gutiérrez-Mañero, F. J., Ramos-Solano, B., Probanza, A.,Mehouachi, J., Tadeo, F. R., Talon, M. (2001): The plant-growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformisproduce high amounts of physiologically active gibberellins.Physiol. Plant. 111, 206–211.

Hall, K. C., Chapman, S. J., Christian, D. G., Jackson, M. B. (1986):Abscisic acid in straw residues from autumn-sown wheat Triticumaestivum. J. Sci. Food Agricult. 37, 219–222.

Harrison, M. J. (1999): Molecular and cellular aspects of the arbus-cular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol.Biol. 50, 219–243.

Härtel, H., Benning, C. (2000): Can digalactosyldiacylglycerolsubstitute for phosphatidylcholine upon phosphate deprivation inleaves and roots of Arabidopsis? Biochem. Soc. Trans. 28,729–732.

Hartung, W. (1996): Trockenheit, in Brunold, C., Rüegsegger, A.,Brändle, R. (eds): Stress bei Pflanzen: Ökologie, Physiologie,Biochemie, Molekularbiologie. Verlag Paul Haupt, Bern, Stuttgart,Wien, pp. 119–131.

Hartung, W., Sauter, A., Turner, N. C., Fillery, I., Heilmeier, H. (1996):Abscisic acid in soils – what is its function and which factors andmechanisms influence its concentration? Plant Soil 184, 105–110.

Henson, I. E. (1984): The heritability of abscisic-acid accumulation inwater stressed leaves of pearl millet Pennisetum americanum.Ann. Bot. 53, 1–12.

Hinsinger, P. (2001): Bioavailability of soil inorganic P in the rhizo-sphere as affected by root-induced chemical changes: A review.Plant Soil 237, 173–195.

Hinsinger, P., Plassard, C., Tang, C. X., Jaillard, B. (2003): Origins ofroot mediated pH changes in the rhizosphere and their responsesto environmental constrains: A review. Plant Soil 248, 43–59.

Hirai, N., Yoshida, R., Todoroki, Y., Ohigashi, H. (2000): Biosynthesisof abscisic acid by the non-mevalonate pathway in plants, and bythe mevalonate pathway in fungi. Biosci. Biotechnol. Biochem. 64,1448–1458.

Höflich, G., Kühn, G. (1996): Promotion of plant growth and nutrientuptake of cruciferous oil- and intercrops by inoculated rhizospheremicroorganisms. Z. Pflanzenernähr. Bodenkd. 159, 575–581.

Hulme, M., Sheard, N. (1999): Climate Change Scenarios forGermany. Climatic Research Unit, Norwich, UK.

Ishikawa, S., Adu-Gyamfi, J. J., Nakamura, T., Yoshihara, T.,Watanabe, T., Wagatsuma, T. (2002): Genotypic variability in phos-phorus solubilizing activity of root exudates by pigeonpea grown inlow-nutrient environments. Plant Soil 245, 71–81.

Itai, C. (1999): Role of phytohormones in plant responses to stress,in Lerner, H. R. (ed.): Plant Responses to Environmental Stress:



from Phytohormones to Genome Reorganization. Marcel Dekker,Inc., New York, Basel, pp. 287–301.

Itai, C., Birnbaum, H. (1996): Synthesis of plant growth regulators byroots, in Waisel, Y., Eshel, A., Kafkafi, U. (eds.): Plant Roots: TheHidden Half. 2nd ed., Marcel Dekker, Inc., New York, Basel, HongKong, pp. 273–284.

Jones, D. L. (1998): Organic acids in the rhizosphere – A criticalreview. Plant Soil 205, 25–44.

Jones, D. L., Hodge, A., Kuzyakov, Y. (2004): Plant and mycorrhizalregulation of rhizodeposition. New Phytol. 163, 459–480.

Karthikeyan, A. S., Varadarajan, D. K., Mukatira, U. T., D’Urzo, M. P.,Damsz, B., Raghothama, K. G. (2002): Regulated expression ofArabidopsis phosphate transporters. Plant Physiol. 130, 221–233.

Khalid, A., Arshad, M., Zahir, Z. A. (2004): Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat.J. Appl. Microbiol. 96, 473–480.

Kozlowski, T. T., Pallardy, S. G. (2002): Acclimation and adaptiveresponses of woody plants to environmental stresses. Bot. Rev.68, 270–334.

Laby, R. J., Kinkaid, M. S., Kim, D., Gibson, S. I. (2000): The Arabi-dopsis sugar-insensitive mutants sis4 and sis5 are defective inabscisic acid synthesis and response. Plant J. 23, 587–596.

Lamont, B. B. (2003): Structure, ecology and physiology of rootclusters: A review. Plant Soil 248, 1–9.

Liu, J., Samac, D. A., Bucciarelli, B., Allan, D. L., Vance, C. P. (2005):Signaling of phosphorus deficiency-induced gene expression inwhite lupine requires sugar and phloem transport. Plant J. 41,257–268.

López-Bucio, J., Nieto-Jacobo, M. F., Ramírez-Rodríguez, V.,Herrera-Estrella, L. (2000): Organic acid metabolism in plants:From adaptive physiology to transgenic varieties for cultivation inextreme soils. Plant Sci. 232, 69–79.

López-Bucio, J., Hernández-Abreu, E., Sánchez-Calderón, L., Nieto-Jacobo, M. F., Simpson, J., Herrera-Estrella, L. (2002): Phosphateavailability alters architecture and causes changes in hormonesensitivity in the Arabidopsis root system. Plant Physiol. 129,244–256.

López-Bucio, J., Cruz-Ramírez, A., Herrera-Estrelle, L. (2003): Therole of nutrient availability in regulating root architecture. Curr.Opin. Plant Biol. 6, 280–287.

Luu, D.-T., Maurel, C. (2005): Aquaporins in a challenging envir-onment: molecular gears for adjusting plant water status. PlantCell Environ. 28, 85–96.

Lynch, J. P., Brown, K. M. (2001): Topsoil foraging: An architecturaladaptation of plants to low phosphorus availability. Plant Soil 237,225–237.

Ma, Z., Bielenberg, D. C., Brown, K. M., Lynch, J. P. (2001): Regu-lation of root hair density by phosphorus availability in Arabidopsisthaliana. Plant Cell Environ. 24, 459–467.

Ma, Z., Baskin, T. I., Brown, K. M., Lynch, J. P. (2003): Regulation ofroot elongation under phosphorus stress involves changes inethylene responsiveness. Plant Physiol. 131, 1381–1390.

Marschner, H., Römheld, V., Horst, W. J., Martin, P. (1986): Root-induced changes in the rhizosphere. Importance for the mineralnutrition of plants. Z. Pflanzenernähr. Bodenkd. 149, 441–456.

Martin, A. C., del Pozo, J. C., Iglesias, J., Rubio, V., Solano, R., de laPena, A., Leyva, A., Paz-Ares, J. (2000): Influence of cytokinins onthe expression of phosphate starvation responsive genes in Arabi-dopsis. Plant J. 24, 559–567.

McCully, M. E., Boyer, J. S. (1997): The expansion of root capmucilage during hydration: III. Changes in water potential andwater content. Physiol. Plant. 99, 169–177.

McLachlan, K. D., De Marco, D. G. (1982): Acid phosphatase activityof intact roots and phosphorus nutrition in plants. III. Its relation tophosphorus garnering by wheat and a comparison with leaf activityas a measure of phosphorus status. Aust. J. Agric. Res. 33, 1–11.

Milborrow, B. V. (2001): The pathways of biosynthesis of abscisicacid in vascular plants: A review of the present state of knowledgeof ABA biosynthesis. J. Exp. Bot. 52, 1145–1164.

Müller, M., Deigle, C., Ziegler, H. (1989): Hormonal interactions in therhizosphere of maize (Zea mays L.) and their effects on plant de-velopment. Z. Pflanzenernähr. Bodenkd. 152, 247–254.

Müller, R., Nilsson, L., Nielsen, L. K., Nielsen, T. H. (2005): Inter-action between phosphate starvation signalling and hexokinase-independent sugar sensing in Arabidopsis leaves. Physiol. Plant.124, 81–90.

Munns, R., King, R. W. (1988): Abscisic acid is not the only stomatalinhibitor in the transpiration stream of wheat plants. Plant Physiol.88, 703–708.

Munns, R., Passioura, J. B., Milborrow, B. V., James, R. A., Close, T.J. (1993): Stored xylem sap from wheat and barley in drying soilcontains an inhibitor with a large molecular size. Plant Cell Environ.16, 867–872.

Nayyar, H., Walia, D. P. (2004): Genotypic variation in wheat in re-sponse to water stress in abscisic acid-induced accumulation ofosmolytes in developing grains. J. Agron. Crop Sci. 190, 39–45.

Neumann, G., Massonneau, A., Langlade, N., Dinkelaker, C.,Römheld, V., Martinoia, E. (2000): Physiological aspects of clusterroot function and development in phosphorus-deficient white lupin(Lupinus albus L.). Ann. Bot. 85, 909–919.

Nguyen, C. (2003): Rhizodeposition of organic C by plants:Mechanisms and controls. Agronomie 23, 375–396.

O’Callaghan, K. J., Dixon, R. A., Cocking, E. C. (2001): Arabidopsisthaliana: A model for studies of colonization by non-pathogenicand plant-growth-promoting rhizobacteria. Aust. J. Plant Physiol.28, 975–982.

Ortiz-Monasterio, J. I., Manske, G. G. B., van Ginkel, M. (2001):Nitrogen and phosphorus use efficiency, in Reynolds, M. P., Ortiz-Monasterio, J. I., McNab, A. (eds.): Application of Physiology inWheat Breeding. CIMMYT, Mexico, D. F., pp. 200–207.

Passioura, J. B. (2002): Soil conditions and plant growth. Plant CellEnviron. 25, 311–318.

Paterson, E. (2003): Importance of rhizodeposition in coupling ofplant and microbial productivity. Eur. J. Soil Sci. 54, 741–750.

Persello-Cartieaux, F., Nussaume, L., Robaglia, C. (2003): Talesfrom the underground: molecular plant-rhizobacteria interactions.Plant Cell Environ. 26, 189–199.

Plaxton, W. C., Carswell, M. C. (1999): Metabolic aspects of thephosphate starvation response in plants, in Lerner, H. R. (ed.):Plant Responses to Environmental Stresses: from Phytohormonesto Genome Reorganization. Marcel Dekker, Inc., New York, Basel,pp. 349–353.

Quarrie, S. A. (1981): Genetic variability and heritability of drought-induced abscisic acid accumulation in spring wheat. Plant CellEnviron. 4, 147–151.

Quarrie, S. A. (1996): New molecular tools to improve the efficiencyof breeding for increased drought resistance. Plant Growth Regul.20, 167–178.

Quarrie, S. A., Laurie, D. A., Zhu, J., Lebreton, C., Semikhodskii, A.,Steed, A., Witsenboer, H., Calestani, C. (1997): QTL analysis tostudy the association between leaf size and abscisic acid accumu-lation in drought rice leaves and comparisons across cereals.Plant Mol. Biol. 35, 155–165.



Raghothama, K. G. (1999): Phosphate acquisition. Annu. Rev. PlantPhysiol. Plant Mol. Biol. 50, 665–693.

Randall, P. J., Hayes, J. E., Hocking, P. J., Richardson, A. E. (2001):Root exudates in phosphorus acquisition by plants, in Ae, N.,Arihara, J., Okada, K., Srinivasan, A. (eds.): Plant Nutrient Acqui-sition. New Perspectives. Springer, Tokyo, Berlin, Heidelberg, NewYork, pp. 71–100.

Rengel, Z. (2002): Genetic control of root exudation. Plant Soil 245,59–70.

Rivier, L., Leonard, J. F., Cottier, J. P. (1983): Rapid effect of osmoticstress on the content and exodiffusion of abscisic acid in Zea maysroots. Plant Sci. Lett. 31, 133–137.

Romera, F. J., Alcantara, E. (2004): Ethylene involvement in theregulation of Fe-deficiency stress responses by Strategy I plants.Funct. Plant Biol. 31, 315–328.

Rubio, G., Zhu, J., Lynch, J. P. (2003): A critical test of the twoprevailing theories of plant response to nutrient availability. Amer.J. Bot. 90, 143–152.

Ryan, P. R., Delhaize, E., Jones, D. L. (2001): Function and mechan-ism of organic anion exudation from plant roots. Annu. Rev. PlantPhysiol. Plant Mol. Biol. 52, 527–560.

Saab, I. N., Sharp, R. E., Pitchard, J., Voetberg, G. S. (1990): In-creased endogenous abscisic acid maintains primary root growthand inhibits shoot growth in maize seedlings at low water poten-tials. Plant Physiol. 93, 109–121.

Sahin, F., Çakmakçi, R., Kantar, F. (2004): Sugar beet and barelyyields relation to inoculation with N2-fixing and phosphate solubi-lizing bacteria. Plant Soil 265, 123–129.

Sauter, A., Hartung, W. (2000): Abscisic conjugates – do they play arole as long distance stress signal in the xylem? J. Exp. Bot. 51,929–935.

Sauter, A., Dietz, K.-J., Hartung, W. (2002): A possible stress physio-logical role of abscisic acid conjugates in root-to-shoot signalling.Plant Cell Environ. 25, 223–228.

Schachtman, D. P., Reid, R. J., Ayling, S. M. (1998): Phosphorusuptake by plants: from soil to cell. Plant Physiol. 116, 447–453.

Schikora, A., Schmidt, W. (2002): Formation of transfer cells and H+-ATPase expression in tomato roots under P and Fe deficiency.Planta 215, 304–311.

Schilling, G., Gransee, A., Deubel, A., Lezovic, G., Ruppel, S.(1998): Phosphorus availability, root exudates, and microbialactivity in the rhizosphere. J. Plant Nutr. Soil Sci. 161, 465–478.

Schulte-Altedorneburg, M., Marx, S., Schneider-Poetsch, H. A. W.,Willenbrink, J. (1989): Quantitative determination and distributionof free and conjugated ABA in sugar beet plants. J. Plant Physiol.135, 52–56.

Schünmann, P. H. D., Richardson, A. E., Smith, F. W., Delhaize, E.(2003): Characterization of the barley phosphate transporter genepromoter, and their potential use as tools for improving plantnutrition, in Rengel, Z. (compiled): Proceedings of Second Interna-tional Symposium on Phosphorus Dynamics in the Soil-PlantContinuum. Perth, Western Australia September 21–26, 2003,University of Western Australia, pp. 132–133.

Schwartz, S. H., Qin, X., Zeevaart, J. A. D. (2003): Elucidation of theindirect pathway of abscisic acid biosynthesis by mutants, genes,and enzymes. Plant Physiol. 131, 1591–1601.

Seo, M., Koshiba, T. (2002): The complex regulation of ABAbiosynthesis in plants. Trends Plant Sci. 7, 41–48.

Sharp, R. E. (2002): Interaction with ethylene: changing views on therole of abscisic acid in root and shoot growth responses to waterstress. Plant Cell Environ. 25, 211–222.

Sharp, R. E., LeNoble, M. E. (2002): ABA, ethylene and the control ofshoot and root growth under water stress. J. Exp. Bot. 53, 33–37.

Sharp, R. E., LeNoble, M. E., Else, M. A., Thorne, E. T., Gherardi, F.(2000): Endogenous ABA maintains shoot growth in tomato inde-pendently of effects on plant water balance: Evidence for an inter-action with ethylene. J. Exp. Bot. 51, 1575–1584.

Sinclair, T. R., Vadez, V. (2002): Physiological traits for crop yield im-provement in low N and P environment. Plant Soil 245, 1–15.

Slovik, S., Daeter, E., Hartung, W. (1995): Compartmental redistri-bution and long-distance transport of abscisic acid (ABA) in plantsas influenced by environmental changes in the rhizosphere – abiomathematical model. J. Exp. Bot. 46, 881–894.

Smithson, P. C., Sanchez, P. A. (2001): Plant nutritional problems inmarginal soils of developing countries, in Ae, N., Arihara, J.,Okada, K., Srinivasan, A. (eds.): Plant Nutrient Acquisition. NewPerspectives. Springer, Tokyo, Berlin, Heidelberg, New York,pp. 32–68.

Spollen, W. G., LeNoble, M. E., Sanmels, T. D., Bernstein, N., Sharp,R. E. (2000): Abscisic acid accumulation maintains maize primaryroots elongation at low water potentials by restricting ethyleneproduction. Plant Physiol. 122, 967–976.

Suzuki, N., Taketa, S., Ichii, M. (2003): Morphological and physiolo-gical characteristics of a root-hairless mutant in rice (Oryza sativaL.). Plant Soil 255, 9–17.

Swindale, L. D., Bidinger, F. R. (1981): Introduction: the humanconsequences of drought and crop research priorities for alle-viation, in Paleg, L. G., Aspinall, D. (eds.): The Physiology andBiochemistry of Drought Resistance in Plants. Academic Press,Sydney, New York, London, Toronto, San Francisco, pp. 1–13.

Tan, B. C., Schwartz, S. H., Zeevaart, J. A. D., McCarty, D. R. (1997):Genetic control of abscisic acid biosynthesis in maize. Proc. Natl.Acad. Sci. 94, 12235–12240.

Tarafdar, J. C., Jungk, A. (1987): Phosphatase activity in the rhizo-sphere and its relation to the depletion of soil organic phosphorus.Biol. Fertil. Soils 3, 199–204.

Taylor, H. F., Smith, T. A. (1967): Production of plant growth inhibitorsfrom xanthophylls: a possible source of dormin. Nature 215,1513–1514.

Teale, W. D., Paponov, I. A., Ditengou, F., Palme, K. (2005): Auxinand the developing root of Arabidopsis thaliana. Plant Physiol.123, 130–138

Ticconi, C. A., Delatorre, C. A., Lahner, B., Salt, D. E., Abel, S.(2004): Arabidopsis pdr2 reveals a phosphate-sensitive checkpointin root development. Plant J. 37, 801–814.

Trewavas, A. (1986): Understanding the control of plant developmentand the role of plant growth substances. Aust. J. Plant Physiol. 13,447–457.

Tuberosa, R., Sanguineti, M. C., Stefanelli, S., Landi, P. (1992):Genotypic variation in abscisic acid (ABA) accumulation in artifi-cially water-stressed maize leaves and its relationship with theABA in drought-stressed field conditions. J. Genet. Breed. 46,331–334.

Uhde-Stone, C., Zinn, K., Liu, J., Miller, S., Reinders, A., Ward, J.,Allan, D., Vance, C. (2003): A MATE transporter gene from phos-phorus (P) deficient white lupine: possible involvement in proteoidroot function, in Rengel, Z. (compiled): Proceedings of SecondInternational Symposium on Phosphorus Dynamics in the Soil-Plant Continuum. Perth, Western Australia, September 21–26,2003, University of Western Australia, pp. 134–135.

Umweltbundesamt (ed.) (2002): Umweltdaten Deutschland 2002.Umweltbundesamt, Berlin, www.umweltbundesamt.de/udd/udd2002.pdf



Vance, C. P., Uhde-Stone, C., Allan, D. L. (2003): Phosphorus acqui-sition and use: critical adaptations by plants for securing a nonre-newable resource. New Phytol. 157, 423–447.

Vessey, J. K. (2003): Plant growth promoting rhizobacteria as bioferti-lizers. Plant Soil 255, 571–586.

Walker, T. S., Bais, H. P., Grotwold, E., Vivanco, J. M (2003): Rootexudation and rhizosphere biology. Plant Physiol. 132, 44–51.

Weyers, J. D. B., Paterson, N. W. (2001): Plant hormones and thecontrol of physiological processes. New Phytol. 152, 375–407.

Wilkinson, S., Davies, W. J. (2002): ABA-based chemical signalling:the co-ordination of responses to stress in plants. Plant CellEnviron. 25, 195–210.

Williams, M. (ed.) (2002): Climate Change: Information Kit. Publishedby the United Nations Environment Programme (UNEP) and theClimate Change Secretariat (UNFCCC), Geneva.

Williamson, L. C., Ribrioux, S. P. C. P., Fitter, A. H., Leyser, H. M. D.(2001): Phosphate availability regulates root system architecture inArabidopsis. Plant Physiol. 126, 875–890.

Wittenmayer, L. (1992): Untersuchungen über die hormonelleSteuerung des Blatt/Rübenkörper-Verhältnisses bei Zuckerrü-benpflanzen (Beta vulgaris L. ssp. vulgaris var. altissima [Doell])unter besonderer Berücksichtigung der Abscisinsäure. PhD thesis,University of Halle, Germany.

Wittenmayer, L. (2001): Untersuchungen zum Rübenkörper-wachstum bei Zuckerrüben (Beta vulagris L. ssp. vulgaris var.altissima [Doell]), in Merbach, W., Wittenmayer, L., Augustin, J.(eds.): Physiologie und Funktion von Pflanzenwurzeln.B. G. Teubner, Suttgart, Leipzig, Wiesbaden, pp. 30–35.

Wittenmayer, L., Schilling, G. (1998): Behaviour of sugar-beet plants(Beta vulgaris L. ssp. vulgaris var. altissima [Doell]) under condi-

tions of changing water supply: abscisic acid as indicator. J. Agron.Crop Sci. 180, 65–72.

Wittenmayer, L., Deubel, A., Wollny, J., Triebswetter, K. (2003): EineKultivierungsmethode zur Untersuchung von Phytohormoneffektenauf Rhizosphärenprozesse, in Merbach, W., Hütsch, B. W., Witten-mayer, L., Augustin, J. (eds.): Prozessregulation in der Rhizo-sphäre. B. G. Teubner, Suttgart, Leipzig, Wiesbaden, pp. 107–114.

Wittenmayer, L., Deubel, A., Merbach, W. (2004): PhysiologischeStressreaktionen bei Kulturpflanzen am Beispiel von Wasser- undPhosphatmangel. Vortr. Pflanzenzücht. 63, 7–21.

Xu, X., Cifre, J., Medrano, H. (2002): Abscisic acid to the nutrientsolution induces a water deficit-like response in Trifolium subter-raneum. Ann. Appl. Biol. 140, 297–304.

Yan, X., Lynch, J. P., Beebe, S. E. (1996): Utilization of phosphorussubstrates by contrasting common bean genotypes. Crop Sci. 36,936–941.

Yan, X., Liao, H., Beebe, S. E., Blair, M. W., Lynch, J. P. (2004): QTLmapping of root hair and acid exudation traits and their relationshipto phosphorus uptake in common bean. Plant Soil 265, 17–29.

Young, I. M. (1995): Variation in moisture contents between bulk soiland the rhizosheath of Triticum aestivum L. cv. New Phytol. 130,135–139.

Younis, M. E., Abbas, M. A., Shukry, W. M. (1994): Salinity andhormone interactions in affecting growth, transpiration and ionicrelations of Phaseolus vulgaris. Biol. Plant. 36, 83–89.

Yu, B., Xu, C., Benning, C. (2002): Arabidopsis disrupted in SQD2encoding sulfolipid synthase is impaired in phosphate-limitedgrowth. Proc. Natl. Acad. Sci. USA 99, 5732–5737.

Zhang, J., Davies, W. J. (1987): Increased synthesis of ABA inpartially dehydrated root tips and ABA transport from roots toleaves. J. Exp. Bot. 38, 2015–2023.



responses to drought and phosphorus deficiency-and phytohormone

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