1. Introduction
Water is one of the most important substances for both plant and animal survival. Plants require water for photosynthesis, nutrient uptake and transportation as well as cooling (Farooq et al., 2009). Plants are sessile organisms and in contrast to most animals they are unable to move when the environment becomes unfavorable. Accordingly, plants have to be able to respond and adapt to the local environmental changes. Since water is essential for plant survival, the ability to tolerate water stress is crucial.
To be able to grow plants need to take up water from the soil and CO2 from the atmosphere and use it in photosynthesis. This is done by CO2 uptake through the stomatal pore, where water is simultaneously transpired. Water transpiration drives the water uptake by the roots and transport through the xylem. When the stomata are open CO2 is taken up while water is transpired. When the stomata are closed little CO2 is taken up and the transpiration is lowered. By opening and closing the stomata plants can regulate the amount of water lost, by sacrificing CO2 uptake, when the environmental conditions are unfavorable.
Water stress can be defined as reduced water availability; either by water scarcity (drought) or osmotic stress (high salt concentrations) or water logging; too much water. Water stress may reduce photosynthesis, respiration and ion uptake, change the metabolic and growth patterns in the plant and in severe cases result in plant death (Jaleel et al., 2009a). In nature water stress is common either for long or short periods of time, depending on the local climate. Most plants therefore have some adaptation or response to enhance the growth and survival rate during water stress and subsequent recovery.
In agriculture and horticulture drought stress is one of the major problems, causing major crop losses every year as well as loss of aesthetic value in ornamentals. In agriculture crop loss is due to reduced numbers of tillers, spikes and grains per plant and reduced grain weight (Farooq et al., 2009). With the global human population rapidly increasing, simultaneously as water scarcity increases, the loss of crop will be even more serious than before. The discovery and development of stress tolerant crops to avoid yield loss during water stress is therefore very important. In the greenhouse industry, energy saving for economic profit is important to be able, but it also affects the plants. To reduce the amount of energy needed for CO2 and heating in the greenhouses, energy-efficient semi-closed greenhouses can be used. In these greenhouses the ventilation is reduced to a minimum, which consequently results in increased relative air humidity inside. This increase in air humidity affects the plants in different ways and might result in plants that are less tolerant to water stress (Torre and Fjeld, 2001).
In this review different plant responses to water stress will be discussed, with most attention to drought and the role for abscisic acid (ABA) as a plant stress hormone. In addition, consequences of plant development under high relative air humidity, which reduces the plants ability to respond to water stress, will be discussed.
2. Plant responses to water stress
Plants growing in deserts or high salinity habitats are all exposed to more or less constant water stress. To survive such conditions plants have developed growth strategies such as increased water use efficiency with C4- or CAM metabolism (Keeley and Rundel, 2003), succulent growth and extensive root systems (Henry et al., 2011). These strategies are good in a dry environment, but in more “favourable” conditions at least some of these plants may, due to lower growth rates, more easily be outcompeted by other less drought tolerant plants. Other adaptations to plant life in dry environments are thick cuticula and wax layers, depressed stomata and high density of trichomes. Thick cuticula and wax layers reduce extra-stomatal transpiration, and depressed stomata and trichomes create a thicker boundary layer outside the stomata, where the humidity gradient is more gradual, thereby reducing the stomatal transpiration.
Plants living in saline environments (e.g. beaches, salt marches) commonly keep a low osmotic potential in their cells, which facilitates water uptake. They usually also have the ability to exclude or excrete salt from their cells to avoid to too high salt concentrations. A variety of perennials commonly avoid water stress during the winter by entering dormancy and often shedding leaves (deciduous woody species) before the onset of the harsh conditions when water is unavailable due to frost. However, plants keeping the leaves on through the winter commonly face water stress in the spring when air temperatures are high while the soil is still frozen.
Even if they do not live in particularly dry places, most plants will occasionally encounter water stress for shorter or longer periods of time. Most of these plants do not have many of the adaptations of desert plants and must respond to the water stress in other ways. When these plants are exposed to water stress, such as drought or saline conditions, to survive they must be able to retain as much water as possible. If the plants are not able to cope with the water stress, they will not be able to survive. The sensitivity and response time to drought differs between different species and slow growing species have been found to be more sensitive (Aasamaa and Sober, 2011). Repeated drought encounters increases the sensitivity to environmental changes that induce stomatal closure, while the sensitivity to changes that induce stomatal opening is decreased (Aasamaa and Sober, 2011). In response to water stress plants have developed several different mechanisms that increase the desiccation tolerance and water retention. These responses can be divided into short term and long term responses (Figure 1).
2.1. Long term responses
During prolonged water stress plants must be able to survive with low water content and maintain a minimum amount of water, through water uptake and retention. To cope with prolonged drought stress plants respond with energy demanding processes that alter the growth pattern, chemical content of the plants and the up or down regulation of genes.
2.1.1. Biochemical changes
When the water availability is reduced, plants change the biochemistry to be able to retain as much water as possible and take up whatever water they can. During water stress plants produce and accumulate compatible solutes such as sugars, polyols and amino acid to lower the osmotic potential in the cells to facilitate water absorption and retention (Xiong and Zhu, 2002). Some of the compatible solutes also contribute to maintaining the conformation of macromolecules by preventing misfolding or denaturation (Xiong and Zhu, 2002). Plants also produce higher levels of the plant stress hormone ABA during water stress and this affects their growth pattern and stress tolerance (details under growth changes and stomatal functioning).
A group of proteins called late embryogenesis abundant like (LEA) proteins are also produced during water stress. These LEA-like proteins are highly hydrophilic, glycine-rich and highly soluble and have been found to be regulated by ABA (Xiong and Zhu, 2002). The LEA-like proteins are thought to act as chaperones, protecting enzymatic activities (Reyes et al., 2005) and preventing misfolding and denaturation of important proteins (Xiong and Zhu, 2002). Some of the LEA-like proteins have similar features as ribosomal proteins and are thought to interact with RNA (Garay-Arroyo et al., 2000).
Decreased transpiration and decreased CO2 and nutrient uptake during water stress result in changes in metabolic pathways such as photosynthesis and respiration, as well as changes in ion uptake, transport and extrusion (Xiong and Zhu, 2002). Some of these changes can lead to oxidative damage. Reactive oxygen species, such as H2O2, O2 -, OH and OH2, are by-products in electron transport chains and have unpaired electrons that can attract electrons from other components. Reactive oxygen species can therefore cause damage to a variety of compounds such as DNA, RNA, proteins, lipids and chlorophyll and thus damage membranes and change cell metabolism and eventually lead to senescence. Many antioxidant systems, both enzymatic and non-enzymatic, are up-regulated in response to the increased reactive oxygen species levels during water stress. These antioxidants scavenge the reactive oxygen species and reduce the oxidative damage. The enzymatic antioxidants, such as superoxide dismutase, peroxidase, ascorbate peroxidase, catalase, polyphenol oxidase and gluthathione reductase can detoxify reactive oxygen species (Prochazkova et al., 2001, Jaleel et al., 2009b). The non-enzymatic anti oxidants, including vitamins (A, C and E), glutathione, carotenoids and phenolic compounds, can scavenge reactive oxygen species by donating an electron or a hydrogen atom (Prochazkova et al., 2001, Jaleel et al., 2009b).
2.1.2. Growth changes
During water stress the water content of the plant decreases, which causes the cells to lose turgor pressure and shrink. The loss of turgor pressure in the cells inhibits turgor dependent activities such as cell expansion, which affects the growth of the whole plant. Some studies show that ABA can function as a signal to reduce leaf growth rate, both when ABA is applied exogenously or generated by water stress (Wilkinson and Davies, 2010). Reduced cell growth during water stress has e.g. been found to decrease the stem length in
To increase water uptake and maintain a minimum osmotic pressure during drought many plants increase their root growth, either deeper or laterally. By increasing the root growth the area for water uptake becomes larger and water further away and deeper in the soil may be reached. This growth response has been found in e.g. maize, madagaskar periwinkle (
2.2. Short term response
When plants suddenly encounter drought it is important to respond as quickly as possible. A faster drought response means that less water is lost and the survival rate of the plants is increased. The most important quick response is stomatal closure. Stomata consist of two guard cells surrounding the stomatal pore. When the stomata are open water is transpired and CO2 enter the leaf through the stomatal pore. During water stress the stomatal pore can be closed to reduce water loss. By closing the stomatal pore the water use efficiency is increased (Farooq et al., 2009), reducing the amount of water lost per CO2 molecule assimilated. Several mechanisms work together to close the stomata, such as hydro passive closure and chemical signals from the plant stress hormone ABA.
Increased levels of ABA also causes increased hydraulic conductivity in the roots and xylem, enabling the plants to transport more water and thereby recover more rapidly after water stress (Kudoyarova et al., 2011).
3. Stomatal functioning
Development of stomata if often considered one of the most important developments in plant evolution (Brodribb and McAdam, 2011). By being environmentally controlled gateways into the plants controlling CO2 uptake and transpiration they are central determinants of photosynthesis, cooling and nutrient uptake (Farooq et al., 2009). To be able to balance CO2 uptake and water transpiration through stomatal movement is therefore an important response to changes in the environmental conditions. Low transpiration due to stomata closure means less cooling of the leaves and less uptake and transportation of nutrients.
3.1. Stomatal signaling and movement
Stomatal closure occur when the two guard cells surrounding the stomatal opening lose turgor pressure and close the opening (Outlaw, 2003). There are many signals that induce stomatal closure, among these the best known signal is probably ABA. In the signaling pathway towards stomatal closure there are several secondary messengers, such as Ca2+, H2O2 and NO (Atkinson et al., 1990, Zhang et al., 2001, Neill et al., 2002, Garcia-Mata and Lamattina, 2009) that contribute to the stomatal closure. Passive loss of turgor pressure also results in stomatal closure.
Since stomatal closure has negative effects on CO2 uptake, photosynthesis, transpirational cooling as well as water and nutrient uptake it is important to close the stomata only when the benefit of water retention outweighs the negative effects. To be able to close the stomata during unfavourable conditions there are several mechanisms and signalling pathways leading to stomatal closure. These pathways can be divided into hydro passive and active stomatal closure (Figure 2).
3.1.1. Hydro passive stomatal closure
Hydro passive stomatal closure occurs when the water evaporation from the guard cells is too low to be balanced by water movement into these cells. The water content in the cells is then rapidly reduced to the extent where the osmotic pressure is reduced and the cells lose turgor pressure and shrink (Luan, 2002). When this happens the guard cells are unable to maintain the shape and the stomatal pore is covered.
Some studies have shown that passive stomatal closure is important in ferns and Lycopods, but not in Angiosperms and Gymnosperms (Franks and Farquhar, 2007, Brodribb and McAdam, 2011). This is because in Angiosperms and Gymnosperms the guard cells closely interact with their subsidiary cells. When the guard cells lose turgor pressure the subsidiary cells also lose turgor pressure and the force from the subsidiary cells pulls the guard cells apart, opening the stomata. This hydro passive opening is called the “wrong-way” response (Franks and Farquhar, 2007). In contrast the guard cells of ferns and Lycopods do not interact closely with their subsidiary cells.
The loss of turgor pressure in the subsidiary cells in these plants does therefore not result in the guard cells being pulled apart. The simultaneous loss of turgor in the guard cells will in these plants be enough to close the stomata.
3.1.2.Active stomatal closure
ABA as well as elevated levels of CO2 activates signalling pathways leading to stomatal closure (Kim et al., 2010). ABA is produced in the roots and leaves during water stress and is transported to the guard cells. ABA is transported into the guard cells by ATP-binding cassette (ABC) transporters that are located in the plasma membrane (Kang et al., 2010). When the ABC transporters are knocked out the ABA uptake is lower, stomata remain more open during drought and the stress tolerance is decreased (Kang et al., 2010). The ABA signals are first recognised by several receptors. PYR/PYL/RCAR (PYRABACTIN RESISTANCE/ PYRABACTIN RESISTANCE –LIKE/REGULATORY COMPONENT OF ABA RESPONCE) proteins have been shown to function as ABA receptors (Klingler et al., 2010). Another protein GCR2 (G protein coupled receptor) has also been shown to be a ABA receptor (Liu et al., 2007).
The size of the stomatal opening is regulated by the turgor pressure and cell volume of the guard cells (Schroeder et al., 2001, Kim et al., 2010). Regulation of stomatal opening is linked to transport of ions and water through channel proteins across the plasma and vacuole membrane (Kim et al., 2010). ABA induces the production of reactive oxygen species (e.g. H2O2), which in turn acts as a trigger for NO production, inhibition of membrane proton pumps and Ca2+ influx across both the plasma and vacuole membranes. H+-ATPases that are hyperpolarizing the plasma membranes must be inhibited to induce ABA mediated stomatal closure (Merlot et al., 2007). The increased Ca2+ levels activate slow and rapid type anion channels, generating an anion efflux from the cells. The anion efflux depolarizes the membrane, which in turn causes K+ efflux through K+ out channels across both the vacuole and the plasma membrane. Simultaneously Ca2+ also inhibits K+ in channels (Wasilewska et al., 2008). Malate is also converted to starch reducing the osmotic potential and turgor pressure further (Kim et al., 2010). The plasma membrane is thus depolarised, the turgor pressure and cell volume reduced and the stomata close (Kim et al., 2010).
4. ABA biosynthesis and metabolism
Increased content of ABA during water stress has been found in all photosynthetic organisms. The biosynthesis of ABA have previously been thought to occur only in the roots, but more recent studies show that ABA is also synthesized in mesophyll cells, vascular tissue and stomata. As stated above increased levels of ABA in leaves induces and regulates stomatal closure, while the increased levels of ABA in roots increase the hydraulic conductivity increasing the water uptake and transportation (Parent et al., 2009). The amount of ABA in the tissue is regulated in several metabolic steps, both in the biosynthesis and inactivation steps.
ABA is synthesized from phytoene (Figure 3), a carotenoid produced from pyruvate and glyceraldehydes-3-phosphate (Cutler and Krochko, 1999, Liotenberg et al., 1999). In the plastids phytoene is converted to ζ-carotene by phytoene desaturase and then to β-carotene, lycopene and zeaxanthin. Zeaxanthin is converted first to antheraxinthin and then to violaxanthin by zeaxanthin epoxidase (ZEP). Violaxanthin is then converted to xanthoxin by 9-cis-epoxycarotenoid dioxygenase (NCED). Xanthoxin is then converted further in the cytosol. The main pathway from xanthoxin to ABA is through abscisic aldehyde. Xanthoxin is then converted to abscisic aldehyde by an enzyme related to a short-chain dehydrogenase/reductase SDR). Abscisic aldehyde is further oxidized to ABA by abscisic aldehyde oxidase (AAO) (Seo and Koshiba, 2002). It has been found that genes regulating at least the last steps in the ABA biosynthesis (NCED and AAO) are the most important and are strongly up regulated during water stress, showing the important role of ABA as a rapid stress response (Qin and Zeevaart, 1999, Seo et al., 2000).
ABA is further regulated by several inactivation pathways (figure 3) (Cutler and Krochko, 1999). There are two main such pathways. The first is inactivation by oxidation. ABA is then oxidized to 8’-hydroxy ABA and subsequently to phaseic acid (PA) and 4’dihydrophaseic acid (DPA). The conversion of ABA to 8’-hydroxy ABA is catalysed by the enzyme (+)-ABA 8’-hydroxylase (Kushiro et al., 2004) and the enzyme phaseic reductase catalyzes the conversion of PA to DPA (Cutler and Krochko, 1999). (+)-ABA 8’-hydroxylase is highly regulated by environmental factors, such as air humidity (Okamoto et al., 2009). The other inactivation pathway is by conjugation to ABA glucose ester, which is hypothesised to be a storage form of ABA (Cutler and Krochko, 1999). This conjugation is catalyzed by ABA glucosyltransferase (Lee et al., 2006). Several experiments provide evidence that ABA glucose ester can be cleaved enzymatically by β-D-glucosidase (Dietz et al., 2000, Lee et al., 2006). The liberated ABA can then induce metabolic and changes and stomatal closure.
5. Stomatal development under high relative air humidity
Plants grown under high relative air humidity have malfunctioning stomata that are unable to close in response to darkness, ABA and desiccation (Fordham et al., 2001). This results in high stomatal conductance and frequent leaf drying. Also, plants grown
The efficiency of stomatal openings for CO2 uptake and water transpiration is not only determined by the size of the opening, but also by the number of stomata (Metwally et al., 1971). More stomata can take up more CO2 and transpire more. In research done in different humidities it has also been found that the number of stomata per leaf increased with development in higher soil humidities, but when calculated as number of stomata per area the number decreased in higher humidities (Metwally et al., 1970, Metwally et al., 1971). The stomatal index, the number of stomata relative to the number of epidermal cells, was also found to increase with soil moisture (Schürmann, 1959). Similar experiments have been preformed with air humidity, increased air humidity results in increased stomatal density (Sciutti and Morini, 1995). The stomatal density has been found to increase in plants with decreased ABA concentrations, which also have increased transpiration (Lake and Woodward, 2008). In
In the greenhouse industry the stomatal functioning and transpiration influences the post harvest quality of the plants. The value of ornamental plants is dependent on the aesthetic condition. Loss of aesthetic value can be due to water stress, where high transpiration rates shorten the shelf life. When ornamental plants are grown in large scale industries it is important to produce stress tolerant plants that have long shelf lives. In greenhouses there is an artificial environment, where the day length, temperature, relative air humidity (RH) and watering regimes are controlled to be able to produce as many plants as possible with as little cost as possible, without reducing the quality of the plants. This has resulted in energy-efficient greenhouses, which conserve energy (CO2 and temperature) by rarely opening the ventilation. This consequently increases the relative humidity inside the greenhouses. Furthermore, much of the plant breeding is done in greenhouses, particularly when it comes to ornamentals.
Roses developed under high relative humidity (>85%) have 6-8 days shorter shelf life and greater water loss than plants grown under lower humidities (Mortensen and Fjeld, 1998; Torre and Fjeld, 2001). When roses are cultivated in high relative humidity environments in greenhouses they develop large, malfunctioning stomata, similar as the malfunctioning stomata produced under
The shorter shelf life of plants developed under high humidity is a major problem in the greenhouse industry. One of the important challenges is therefore to find new environmental regimes that save energy, but still produce high quality and stress tolerant plants. When plants grown in high relative humidity are treated with a 6 hour low humidity period in the middle of every day, the stomata remain functional (Mortensen et al., 2007, Pettersen et al., 2007). Similarly using 18 hour light period instead of 24 hours also result in more water retention and longer shelf life in roses (Mortensen et al., 2007).
Plants grown under constant high relative humidity contain less ABA than plants grown under lower relative humidities and some of the stomata of these plants are larger and malfunctioning (Nejad and van Meeteren, 2005, 2007). One of the main hypotheses explaining the malfunctioning stomata in high humidity is development with low ABA concentrations (Nejad and van Meeteren, 2007, Okamoto et al., 2009). If the plants developed under high relative humidities are treated with ABA during development, the stomata respond as if they were developed under lower relative humidities (Nejad and van Meeteren, 2007). In plants moved from high humidity to lower humidities regained stomatal functioning in leaves that were still actively expanding, but not in fully developed leaves (Nejad and van Meeteren, 2008). Similarly if leaves developed under high relative humidity were given ABA application, the stomatal functioning was restored in young expanding leaves, but not in fully developed leaves (Nejad and van Meeteren, 2008).These experiments implicate that ABA is involved in the development of functioning and malfunctioning stomata, although there is also contradicting results. In
ABA application in lower concentrations, applied to plants can reduce transpiration rate and increase the shelf life of
6. Conclusion
The ability of plants to be able to regulate the size of the stomatal opening is a very important mechanism to control water loss and survive. This ability is especially important during water stress, when loss of water can have serious consequences for the plants. Water stress can cause reduced growth and in severe cases plant death. To minimize the negative effects of water stress the plants respond by changing their growth pattern, producing stress proteins and chaperones, up-regulation of anti-oxidants, accumulation of compatible solutes, increasing the amount of transporters involved in water and ion uptake and transport and by closing the stomata. If the plants are unable to quickly respond to water stress, by closing the stomata and thereby conserve as much water as possible, the consequences are more severe and plants wilt and die more quickly. This is a major problem in plant propagation of ornamentals. Plants developed under high relative air humidity develop malfunctioning stomata, which are unable to close in response to water stress. When these plants are later placed in dryer conditions they quickly lose their ornamental value and wilt. Treatments with ABA or periods of high temperature or low relative air humidity during development can offset this malfunctioning and produce functioning stomata, even in high humidity.
References
- 1.
Assmann S. M. Snyder J. A. Lee Y. R. J. 2000 ABA-deficient (aba1) and ABA-insensitive (abi1-1, abi2-1) mutants of Arabidopsis have a wild-type stomatal response to humidity . Cell and Environment23 387 395 - 2.
Atkinson C. J. Mansfield T. A. Mc Ainsh M. R. Brownlee C. Hetherington A. M. 1990 Interactions Of Calcium With Abscisic-Acid In The Control Of Stomatal Aperture. Biochemie Und Physiologie Der Pflanzen186 333 339 - 3.
Brainerd K. E. Fuchigami L. H. 1982 Stomatal functioning of invitro and greenhouse apple leaves in darkness, mannitol, ABA and CO2. Journal of Experimental Botany33 388 392 - 4.
Brodribb T. J. Mc Adam S. A. M. 2011 Passive Origins of Stomatal Control in Vascular Plants .331 582 585 - 5.
Cutler A. J. Krochko J. E. 1999 Formation and breakdown of ABA .4 472 478 - 6.
Dietz K. J. Sauter A. Wichert K. Messdaghi D. Hartung W. 2000 Extracellular beta-glucosidase activity in barley involved in the hydrolysis of ABA glucose conjugate in leaves. 51 937 944 - 7.
Djibril S. Mohamed O. K. Diaga D. Diegane D. Abaye B. F. Maurice S. Alain B. 2005 Growth and development of date palm (Phonix dactylifera L.) seedlings under drought and salinity stresses. African Journal of Biotechnology4 968 972 - 8.
Farooq M. Wahid A. Kobayashi N. Fujita D. Basra S. M. A. 2009 Plant drought stress: effects, mechanisms and management .29 185 212 - 9.
Fordham M. C. Harrison-Murray R. S. Knight L. Evered C. E. 2001 Effects of leaf wetting and high humidity on stomatal function in leafy cuttings and intact plants of Corylus maxima .113 233 240 - 10.
Franks P. J. Farquhar G. D. 2007 The mechanical diversity of stomata and its significance in gas-exchange control. 143 78 87 - 11.
Gan Y. Zhou L. Shen Z. J. Shen Z. X. Zhang Y. Q. Wang G. X. 2010 Stomatal clustering, a new marker for environmental perception and adaptation in terrestrial plants .51 325 336 - 12.
Garay-Arroyo A. Colmenero-Flores J. M. Garciarrubio A. Covarrubias A. A. 2000 Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit .275 5668 5674 - 13.
Garcia-Mata C. Lamattina L. 2009 Nitric Oxide Induces Stomatal Closure and Enhances the Adaptive Plant Responses against Drought Stress (126 pg1196 F , 2001). 150: 531-531 - 14.
Giovannelli A. Deslauriers A. Fragnelli G. Scaletti L. Castro G. Rossi S. Crivellaro A. 2007 Evaluation of drought response of two poplar clones (Populus x canadensis Monch’I-214’ and P-deltoides Marsh.’Dvina’) through high resolution analysis of stem growth. 58 2673 2683 - 15.
Gu M. M. Robbins J. A. Rom C. R. 2007 The role of ethylene in water-deficit stress responses in Betula papyrifera marsh. Hortscience42 1392 1395 - 16.
Henry A. Gowda V. R. P. Torres R. O. Mc Nally K. L. Serraj R. 2011 Variation in root system architecture and drought response in rice (Oryza sativa): Phenotyping of the OryzaSNP panel in rainfed lowland fields .120 205 214 - 17.
Heuer B. Nadler A. 1995 Growth and development of potatoes under salinity and water-deficit .46 1477 1486 - 18.
Hronkova M. Zahradnickova H. Simkova M. Simek P. Heydova A. 2003 The role of abscisic acid in acclimation of plants cultivated in vitro to ex vitro conditions .46 535 541 - 19.
Jaleel C. A. Manivannan P. Lakshmanan G. M. A. Gomathinavaam M. Panneerselvam R. 2008 Alterations in morphological parameters and photosynthetic pigment responses of Catharanthus roseus under soil water deficits . Colloids and Surfaces B-Biointerfaces61 298 303 - 20.
Jaleel C. A. Manivannan P. Wahid A. Farooq M. Al-Juburi H. J. Somasundaram R. Panneerselvam R. 2009a Drought Stress in Plants: A Review on Morphological Characteristics and Pigments Composition .11 100 105 - 21.
Jaleel C. A. Riadh K. Gopi R. Manivannan P. Ines J. Al-Juburi H. Chang-Xing Z. Hong-Bo S. Panneerselvam R. 2009b Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints .31 427 436 - 22.
Joshi P. Joshi N. Purohit S. D. 2006 Stomatal characteristics during micropropagation of Wrightia tomentosa .50 275 278 - 23.
Kang J. Hwang J. U. Lee M. Kim Y. Y. Assmann S. M. Martinoia E. Lee Y. 2010 PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid .107 2355 2360 - 24.
Keeley J. E. Rundel P. W. 2003 Evolution of CAM and C-4 carbon-concentrating mechanisms. International Journal of Plant Sciences 164: S55 -S77 - 25.
Kim J. van Iersel M. W. 2011 Abscisic acid drenches can reduce water use and extend shelf life of Salvia splendens .127 420 423 - 26.
Kim T. H. Bohmer M. Hu H. H. Nishimura N. Schroeder J. I. 2010 Guard Cell Signal Transduction Network: Advances in Understanding Abscisic Acid, CO2, and Ca2+ Signaling. In ,61 Vol 61. Annual Reviews, Palo Alto,561 591 - 27.
Klingler J. P. Batelli G. Zhu J. K. 2010 ABA receptors: the START of a new paradigm in phytohormone signalling .61 3199 3210 - 28.
Kudoyarova G. Veselova S. Hartung W. Farhutdinov R. Veselov D. Sharipova G. 2011 Involvement of root ABA and hydraulic conductivity in the control of water relations in wheat plants exposed to increased evaporative demand .233 87 94 - 29.
Kushiro T. Okamoto M. Nakabayashi K. Yamagishi K. Kitamura S. Asami T. Hirai N. Koshiba T. Kamiya Y. Nambara E. 2004 The Arabidopsis cytochrome 450CYP707A encodes ABA 8’-hydroxylases: key enzymes in ABA catabolism. Embo Journal 23: 1647-1656 - 30.
Lake J. A. Woodward F. I. 2008 Response of stomatal numbers to CO2 and humidity: control by transpiration rate and abscisic acid. 179 397 404 - 31.
Lee K. H. Piao H. L. Kim H. Y. Choi S. M. Jiang F. Hartung W. Hwang I. Kwak J. M. Lee I. J. 2006 Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid .126 1109 1120 - 32.
Liotenberg S. North H. Marion-Poll A. 1999 Molecular biology and regulation of abscisic acid biosynthesis in plants .37 341 350 - 33.
Liu X. G. Yue Y. L. Li B. Nie Y. L. Li W. Wu W. H. Ma L. G. 2007 A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid .315 1712 1716 - 34.
Luan S. 2002 Signalling drought in guard cells . Cell and Environment25 229 237 - 35.
Merlot S. Leonhardt N. Fenzi F. Valon C. Costa M. Piette L. Vavasseur A. Genty B. Boivin K. Muller A. Giraudat M. Leung J. 2007 Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure. Embo Journal26 3216 3226 - 36.
Metwally A. W. Beck G. E. Struckme Be. 1971 Density and behavior of stomata of Pelargonium hortorum- Grown under 3 soil moisture regimes. Journal of the American Society for Horticultural Science96 31 -& - 37.
Metwally A. W. Struckme Be. Beck G. E. 1970 Effect of 3 soil moisture regimes on growth and anatomy of Pelargonium hortorum. Journal of the American Society for Horticultural Science95 803 -& - 38.
Mortensen L. M. Fjeld T. 1998 Effects of air humidity, lighting period and lamp type on growth and vase life of roses .73 229 237 - 39.
Mortensen L. M. Pettersen R. I. Gislerod H. R. 2007 Air humidity variation and control of vase life and powdery mildew in cut roses under continuous lighting .72 255 259 - 40.
Muller R. Stummann B. M. Andersen A. S. Serek M. 1999 Involvement of ABA in postharvest life of miniature potted roses .29 143 150 - 41.
Neill S. J. Desikan R. Clarke A. Hancock J. T. 2002 Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells .128 13 16 - 42.
Nejad A. R. van Meeteren U. 2005 Stomatal response characteristics of Tradescantia virginiana grown at high relative air humidity .125 324 332 - 43.
Nejad A. R. van Meeteren U. 2007 The role of abscisic acid in disturbed stomatal response characteristics of Tradescantia virginiana during growth at high relative air humidity. 58 627 636 - 44.
Nejad A. R. van Meeteren U. 2008 Dynamics of adaptation of stomatal behaviour to moderate or high relative air humidity in Tradescantia virginiana. 59 289 301 - 45.
Okamoto M. Tanaka Y. Abrams S. R. Kamiya Y. Seki M. Nambara E. 2009 High Humidity Induces Abscisic Acid 8’-Hydroxylase in Stomata and Vasculature to Regulate Local and Systemic Abscisic Acid Responses in Arabidopsis. 149 825 834 - 46.
Outlaw W. H. 2003 Integration of cellular and physiological functions of guard cells. Critical Reviews in Plant Sciences22 503 529 - 47.
Parent B. Hachez C. Redondo E. Simonneau T. Chaumont F. Tardieu F. 2009 Drought and Abscisic Acid Effects on Aquaporin Content Translate into Changes in Hydraulic Conductivity and Leaf Growth Rate: A Trans-Scale Approach. 149 2000 2012 - 48.
Park J. E. Park J. Y. Kim Y. S. Staswick P. E. Jeon J. Yun J. Kim S. Y. Kim J. Lee Y. H. Park C. M. 2007 GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis .282 10036 10046 - 49.
Petropoulos S. A. Daferera D. Polissiou M. G. Passm H. C. 2008 The effect of water deficit stress on the growth, yield and composition of essential oils of parsley .115 393 397 - 50.
Pettersen R. I. Moe R. Gislerod H. R. 2007 Growth of pot roses and post-harvest rate of water loss as affected by air humidity and temperature variations during growth under continuous light .114 207 213 - 51.
Pompodakis N. E. Joyce D. C. Terry L. A. Lydakis D. E. 2004 Effects of vase solution pH and abscisic acid on the longevity of cut’Baccara’ roses. Journal of Horticultural Science & Biotechnology79 828 832 - 52.
Prochazkova D. Sairam R. K. Srivastava G. C. Singh D. V. 2001 Oxidative stress and antioxidant activity as the basis of senescence in maize leaves .161 765 771 . - 53.
Qin X. Q. Zeevaart J. A. D. 1999 The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean .96 15354 15361 - 54.
Ren J. Dai W. R. Xuan Z. Y. Yao Y. N. Korpelainen H. Li C. Y. 2007 The effect of drought and enhanced UV-B radiation on the growth and physiological traits of two contrasting poplar species .239 112 119 - 55.
Reyes J. L. Rodrigo M. J. Colmenero-Flores J. M. Gil J. V. Garay-Arroyo A. Campos F. Salamini F. Bartels D. Covarrubias A. A. 2005 Hydrophilins from distant organisms can protect enzymatic activities from water limitation effects in vitro .28 709 718 - 56.
Sankar B. Jaleel C. A. Manivannan P. Kishorekumar A. Somasundaram R. Panneerselvam R. 2008 Relative efficacy of water use in five varieties of Abelmoschus esculentus (L.) Moench. under water-limited conditions . Colloids and Surfaces B-Biointerfaces62 125 129 - 57.
Santamaria J. M. Davies W. J. Atkinson C. J. 1993 Stomata of micropropagated Delphinium plants respond to ABA, CO2, light and water potential, but fail to close fully. 44 99 107 - 58.
Schroeder J. I. Allen G. J. Hugouvieux V. Kwak J. M. Waner D. 2001 Guard cell signal transduction .52 627 658 - 59.
Sciutti R. Morini S. 1995 Water-loss and photosynthesis of plum plantlets is influenced by relative-humidity during rooting in-vitro . Journal of Horticultural Science70 221 228 - 60.
Seo M. Koshiba T. 2002 Complex regulation of ABA biosynthesis in plants. 7 41 48 - 61.
Seo M. Peeters A. J. M. Koiwai H. Oritani T. Marion-Poll A. Zeevaart J. A. D. Koornneef M. Kamiya Y. Koshiba T. 2000 The Arabidopsis aldehyde oxidase 3 (AA03) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proceedings of the National Academy of Sciences of the United States of America97 12908 12913 - 62.
Specht J. E. Chase K. Macrander M. Graef G. L. Chung J. Markwell J. P. Germann M. Orf J. H. Lark K. G. 2001 Soybean response to water: A QTL analysis of drought tolerance. Crop Science41 493 509 - 63.
Torre S. Fjeld T. 2001 Water loss and postharvest characteristics of cut roses grown at high or moderate relative air humidity .89 217 226 - 64.
Torre S. Fjeld T. Gislerod H. R. Moe R. 2003 Leaf anatomy and stomatal morphology of greenhouse roses grown at moderate or high air humidity . Journal of the American Society for Horticultural Science128 598 602 - 65.
Trachsel S. Stamp P. Hund A. 2010 Effect of high temperatures, drought and aluminum toxicity on root growth of tropical maize (Zea mays L.) seedlings .55 249 260 - 66.
Wasilewska A. Vlad F. Sirichandra C. Redko Y. Jammes F. Valon C. Frey N. F. D. Leung J. 2008 An update on abscisic acid signaling in plants and more. 1 198 217 - 67.
Waterland N. L. Campbell C. A. Finer J. J. Jones M. L. 2010a Abscisic Acid Application Enhances Drought Stress Tolerance in Bedding Plants .45 409 413 - 68.
Waterland N. L. Finer J. J. Jones M. L. 2010b Abscisic Acid Applications Decrease Stomatal Conductance and Delay Wilting in Drought-stressed Chrysanthemums .20 896 901 - 69.
Wilkinson S. Davies W. J. 2010 Drought, ozone, ABA and et hylene: new insights from cell to plant to community. Plant Cell and Environment33 510 525 - 70.
Xiong L. Zhu J. K. 2002 Molecular and genetic aspects of plant responses to osmotic stress .25 131 139 - 71.
Zhang X. Zhang L. Dong F. C. Gao J. F. Galbraith D. W. Song C. P. 2001 Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba .126 1438 1448 - 72.
Aasamaa K. Sober A. 2011 Stomatal sensitivities to changes in leaf water potential, air humidity, CO2 concentration and light intensity, and the effect of abscisic acid on the sensitivities in six temperate deciduous tree species. 71 72 78