Advanced studies on adaptation of desert shrubs to environmental stress

HaiXia Huang , Gang Wang , NianLai Chen

1. College of Resources and Environmental Sciences, Gansu Agricultural University, Lanzhou 730070, China

2. College of Forestry, Gansu Agricultural University, Lanzhou 730070, China

3. College of Life Sciences, Lanzhou University, Lanzhou 730000, China

Advanced studies on adaptation of desert shrubs to environmental stress

HaiXia Huang1,2, Gang Wang3, NianLai Chen1*

1. College of Resources and Environmental Sciences, Gansu Agricultural University, Lanzhou 730070, China

2. College of Forestry, Gansu Agricultural University, Lanzhou 730070, China

3. College of Life Sciences, Lanzhou University, Lanzhou 730000, China

The combined stress of drought, high temperature and excessive light characterizes the desert area. In order to survive the desert habitat, desert shrubs have evolved a number of special eco-physiological mechanisms to resist environmental stress during long-term evolution. In this paper, adaptation mechanisms of desert shrubs to environmental stress are reviewed in terms of morphological structure, water potential, photosynthesis and water use efficiency, transpiration and stomatal conductance, osmotic adjustment and anti-oxidation protection. In addition, some suggestions for future research are proposed.

desert shrub; drought; high temperature; excessive light; eco-physiology

1. Introduction

Desert areas represent little precipitation, high temperature and intense radiation. Deserts contain sparse vegetation consisting mainly of super-xerophytic, semi-tree form,semi-shrub, shrub or xerophytic succulent plants. In a desert ecosystem, plant gas exchange or productivity is often impacted by drought, excessive light or high temperature at some stages (Jiang and Zhu, 2001a). High temperature stress has the effect of intensifying water stress and water stress tends to intensify injury of plants from high temperature(Liuet al., 2005). To adapt to the environment, desert plants have evolved a set of mechanisms during long-term evolution such as morphological structure, water eco-physiological character, physiological and biochemical reaction, photosynthetic apparatus and protoplast structure(Larcher, 1980). Numerous studies have suggested that desert shrubs adapt to the environment by changing tissue water content and existing water state inside the cell, and adjusting water potential, transpiration intensity, stomatal conductance and water use efficiency, osmotic adjustment and metabolism (Zhao and Huang, 1981; Wang and Ma, 1999;Zhou, 2001; Gonget al., 2005; Xu and Li, 2005). These studies focused on the physiological response ofTamarix hohhenackeri,Calligonum caputmedusaeandHaloxylon ammoendronto high temperature, and photosynthetic characteristics ofArtemisia ordosica,Hedysarum fruticosumandSalix pasmmoplyllaunder high temperature and light conditions have enriched the study on plant anti-stress physiology and provided a basis for ecological restoration in desert areas (Jiang and Zhu, 2001a; Zhou ZBet al.,2005). This paper aims to summarize the countermeasures and mechanisms of desert shrubs to drought, high temperature and radiation.

2. Morphological adaptation

2.1. Leaf adaptation

Leaves are the main plant organ for water loss and pho-tosynthesis and are very sensitive to extreme temperature.Plants can produce diverse morphological variations to adjust the relationship between water evaporation and photosynthesis to maintain proper temperature. Common traits of desert shrub leaves are small surface area,well-developed palisade tissue, thick cuticle and sunken stomata, thus reducing water loss (Liuet al., 1987; Wanget al., 1991). The leaf anatomical structure ofCaraganashows a regular gradient change in its distribution, and in the arid region of northwest China drought-resistant characters are well-developed, including a tendency for smaller leaf area, well developed palisade tissue, intercellular spaces tending to become smaller, well developed epidermal hairs covering the leaf surface, and stronger cutinization, and a progressive development of stronger cutinization, conducting tissue and mechanical tissue in the veins(Yanet al., 2002). In order to adapt to environmental stress,desert shrubs have evolved numerous strategies such as protection, conservation, and tolerance (Liu, 1982).Nitraria tangutorum,Ammopiptanthus mogolicus,A. ordosicaandReaumuria soongoricahave thick cuticle or wax coat on the epidermis, thick epidermal hairs, and sunken stomata (Liu, 1982; Jiang, 2000; Huet al., 2006; Shan and He, 2007), which reduces water loss and intense radiation,characters belonging to the protection strategy.Haloxylon ammodendronandC. mongolicumpossess degraded leaves such that photosynthesis is performed in the green stems,the surface-to-volume ratio ofZ. xanthoxylonis 1:3, which can maximally decrease lighted areas and water loss using limited water (Fahn, 1964), thus adopting conservation strategy. Some desert shrubs can store large volumes of water in mesophyll cells or by some inclusion to restrain drought. For example,N. tangutorum,Peganum harmalaandA. ordosicahave water-saving tissue taking up 70% of the leaf thickness (Wanget al., 1983). In mesophyll and water storage tissue ofH. ammodendronsome crystal-containing cells exist, while numerous mucilage cells exist forC. mongolicum. This can improve plant water-retention and water absorption, providing a relatively wet micro-environment for surrounding photosynthetic cells (Suet al., 2005). Mucilage cells or jelly inHedysarumscoparium,Atraphaxisbracteata,Alhagi pseudalhagiandApocynum venetumcan increase osmotic pressure, which improves water-retention capacity (Jiang,2004).

2.2. Stem adaptation

Desert plants can decrease water loss and improve photosynthesis by increasing water-storing parenchyma cells, forming abnormal structures, and developing chloroplast in cortex cells (Huet al., 2006). Many desert shrubs have developed a periderm, thick cuticle or epidermal hairs,and commonly have green assimilation tissue in the cortex near the epidermis, thus improving photosynthetic efficiency such as inA. mongolicusandZ. xanthoxylon(Songet al., 1997; Zhang DYet al., 2003; Jiang, 2004; Huet al.,2006). Many desert shrubs possess well-developed pith with water-storing function, thus preventing vascular tissue from being exposed to drought (Huanget al., 1997), and crystals exist in cortex and pith cells (Maet al., 1997).Assimilating branches have a thick cortex and well-developed water tissue generally with crystals in the cells. The assimilating stems ofH. ammodendroncontain 7-9 large water cells inside the cortex with crystals in the pith cells, and mucilage cells in stems ofH. scoparium,A.pseudalhagi,H. ammodendronandR. soongorica(Li Z and Li R, 1981; Huanget al., 1997; Denget al., 1998), which helps in storing nutrients, improving osmotic pressure, and water-retaining capacity. Some shrubs such asH. ammodendron,Z. xanthoxylon,Salsda ruthenica,Ceratoides lateensandA. mongolicusform abnormal vascular tissue in the stem, intensifying translocation which is useful for photosynthesis of green parenchymal tissue in the cortex(Zhuet al., 1992; Huet al., 2006). Well-developed mechanical tissue and sclerenchyma around the vascular cylinder provide good support and avoid drought (Zhang DYet al.,2003). Sclerenchyma in stems ofC. lateensandP. harmalais useful for phloem to avoid damage from high temperature,intense radiation and drought (Huanget al., 1997).

2.3. Root adaptation

The range and depth of root distribution have an important effect on plant drought-resistance (Wanget al.,1991). Desert shrubs generally have a well-developed root system and high root/shoot ratio (Liuet al., 2001; Niuet al., 2003; Zhang DYet al., 2003; Jiang and Li, 2008). For instance,A. mongolicusandTetraena mongolicaare taproot plants with a stout main root and numerous developed lateral roots and the growth rate of underground to aboveground structures is 10 to 14 (Liuet al., 2001).Tamarix chinensiscan not only absorb underground water by deep roots but also obtain water from unsaturated areas in the soil (Horton and Clark, 2001). The roots ofA. pseudalhagican reach 15 meters covering 62.3 m2, absorbing underground water to support transpiration of aboveground structures (Denget al., 2002a). Desert shrubs have numerous adaptive characteristics in root anatomic structure such as abnormal vascular inH. ammodendron,P. harmala,C. lateens,S. ruthenicaandSalsola passerine(Jiang, 2004)and developed phellem layer in root secondary structures ofC. mongolicum,H. scoparium,Caragana korshinskiiandH.fruticosum(Anet al., 1996), which prevents damage from high temperature and water loss by reverse osmotic pressure. Some shrubs have specific organs such as root cover inA. mongolicusand sandy cover at the end of lateral roots ofN. tangutorumwhich are effective in retaining water,resisting drought and high temperature. Crystal cells and mucilage cells in roots ofA. mongolicusandH. scopariumcan enhance water-retention capacity (Huanget al., 1997;Huet al., 2006).

3. Physiological and bio-chemical adaptation

3.1. Water potential

Water potential is an important indicator representing plant water status, and its value indicates the possibility of plants to absorb water from soil or nearby cells (Zenget al.,2002). Desert shrubs maintain high tissue water potential by limiting water loss or absorbing water to delay dehydration (Luo and Li, 2005). Under the same soil water content,water potential of assimilating shoots ofH. ammodendronis lower thanC. korshinskii,H. scopariumandH. fruticosumwith a minimal value of -31.48 MPa (Yang and Dong, 1994). A feature of drought tolerance forR. soongorica,T. chinensisandC. korshinskiiis low water potential(Feng, 1995; Liet al., 2005), which is helpful in absorbing soil water and maintaining hydrological balance (Tuomela,1997; Marigoet al., 2000; Liet al., 2002).C. caputmedusecan maintain a high water potential to delay dehydration by stomatal regulation (Denget al., 2002a) andA. ordosicacan endure drought by high water potential (Liet al.,2005).

3.2. Photosynthetic characteristics

Photosynthesis is a physiological process sensitive to environmental change. Generally, plant photosynthesis is limited under drought and high temperature with decreasing net photosynthetic rate (Pn) and maintaining relatively higher photosynthetic rate for plants with higher resistance(Heet al., 2005). Leaves ofH. fruticosumandA. ordosicaexhibited higherPnand stomatal conductance (Gs) than was observed inS. pasmmoplylla, especially under very high leaf temperature (＞46 °C) and high photosynthetic active radiation (PAR) (＞2,100 µmol/(m2·s)), showing a higher resistance to high temperature and intense radiation(Jiang and Zhu, 2001a). Light compensation and saturation point, and optimum temperature for photosynthesis ofC.microphylladistributed in sub-humid and semi-arid areas were all lower than those ofCaragana stenophylladistributed in semi-arid and extremely arid areas. This demonstrates that the photosynthetic system ofC. stenophyllais adapted to intense radiation, high temperature and arid regions better than that ofC. microphylla(Maet al., 2004).Photosynthetic characteristics formed possibly because leaves ofC. microphylaare covered with green villi, while leaves ofC. stenophyllahave off-white villi. Desert shrubs generally have high water use efficiency by reducingPn(Filellaet al., 1998). Species such asS. collina,A. ordosicaandC. microphyllapossessing the C4photosynthetic pathway or nitrogen fixation ability have a higherPn(Liuet al., 2003).Caraganaplants in desert areas have adopted low transpiration and high photosynthesis water-saving countermeasures (Maet al., 2003). Midday depression is an important adaptive strategy forH. ammodendronassimilating shoots to avoid water loss under a desert environment (Jianget al., 2001).Artemisia ordosicais more adaptable to the Shapotou area environment, with strong photo flux density, high temperature and low humidity thanC. korshinskiiandPnwas about three times that ofC.korshinskii, which is possibly related to higherGsand carboxylation efficiency of mesophyll cells ofA. ordosica(Shiet al., 2007). ThePnofA. sparsilolia,C. caput-medusaeandTamarix ramosissimaincreased largely over 30 °C showing that desert plants can shift their temperature niches to higher ones in a higher-temperature environment (Denget al., 2002b).

Plant photosynthesis tends to be impacted by higher temperature and strong irradiance through affecting photo-chemical efficiency and activity of photosynthetic enzymes especially photosystem II (PS II), resulting in excessive excitation energy and inactivation, and even irreversible damage to PS II center. Chloroplast possess adaptive mechanisms such as photo-respiration, xanthophyll cycle and anti-oxidation protection, shifting PS II from thermo-sensitive status to thermo-tolerant state under moderate and high temperature conditions (Havaux, 1995).Light stress can cause photo-inhibition characterized by a decrease of maximal photochemical efficiency of PS II(Fv/Fm) and photosynthetic efficiency (Songet al., 2008).The indicatorFv/Fmcan be used to evaluate adaptation of plants to the environment. This parameter changes little under non-stress, while decreasing after photo-inhibition(Demattoset al., 1997; Zhang Set al., 2003). Midday depression ofFv/Fmis common in areas characterized by aridity, high temperature and strong radiation, which is caused by intense light and exacerbated by drought and high temperature (Correiaet al., 1999; Jiang and Zhu,2001b; Liu and Zhao, 2009). TheFv/Fmof plants possessing C3photosynthetic pathway are about 0.832.Fv/FmofC. korshinskiiin desert areas is about 0.832, but that ofCaragana roborovoskyiwas much lower than 0.832 indicating thatC. korshinskiiis better adapted to a desert environment (Searanoet al., 2001).

3.3. Stomatal conductance and transpiration

Transpiration and stomatal conductance are main factors affecting plant water use efficiency. Xerophytes can obtain water by maintaining low water potential and absorbing water through developed roots, while also avoiding water loss through stomatal regulation. The initial response of leaves to drought stress is possibly to regulate stomatal aperture. With increasing stress of gradual leaf water lose,water potential decreases,Gsreduces and stomatal resistance increases leading to a decline of the photosynthetic rate, while the increase of stomatal resistance can alleviate damage of drought stress to photosynthetic organs(Guanet al., 1995). In general, desert shrubs can close stomata to reduce transpiration when exposed to drought stress around noon, but which may result in temperature rise, impacting photosynthesis (Li and Tang, 2006).Calligonum mongolicumpossess features of high transpiration and high water use efficiency, avoiding damage from high temperature by maximum transpiration (Gonget al., 2005). Transpiration ofC. intemediaappears as a one-peak curve and stomatal are closed from midday till sunset under a water deficit (Donget al., 1994).Caragana korshinskiipossess low transpiration in arid environments which is possible because the leaves are covered with villi possessing high light reflection and low light absorption.Additionally, low temperature is useful for avoiding damage from high temperature and intense light, decreasing water loss by transpiration and improving water-retaining capacity, which accounts for whyC. korshinskiihas high adaptivity to strong radiation and high temperature (Feng,1995; Ma, 2004).GsofH. scopariumis represented as periodic oscillations called stomatal oscillations, which not only decreases transpiration and improves water use efficiency, but barely has an impact on the photosynthetic rate(Zhanget al., 1996).

Water use efficiency (WUE) is a comprehensive indicator representing the capacity to assimilate CO2and H2O to produce organic matter. Short-term water use efficiency can be obtained by measuring the photosynthetic rate and transpiration rate. WUE tends to increase in order of wetland, lowland, fixed sand dune and shifting sand dune, and species of Leguminosae, Gramineae and Chenopodiaceae with C4pathway or nitrogen fixation capacity generally have a higher WUE (Jiang and He, 1999). Plants increase WUE by decreasing transpiration more than the photosynthetic rate (Guoet al., 2004). Plant leaves with C4pathway possess typical Kranz structure, and their WUE are higher than those of C3plants under high temperature, strong light and dry conditions (Liuet al., 2005). WUE of main shrubs in the desert area of northwest China can be ranked in the order ofC. mongolicum＞H. ammodendron＞T. chinensis＞H. scopariumduring the growing season (Jin, 2005).δ13C of leaves can indirectly indicate plant long-term WUE and plants with higher values of δ13C would possess higher WUE (Farquharet al., 1988). Based on δ13C values,long-term WUE ofC. mongolicumandH. ammodendronwith C4pathway were higher than those ofH. scoparium,C. korshinskiiandNitraria sphaerocarpawith C3pathway(Suet al., 2003).

3.4. Osmotic regulation

Osmotic regulation is a main mechanism by which plants adapt to an adverse environment (Peltieret al.,1997). Plants actively accumulate solutes in cells, reduce osmotic potential and produce osmotic regulation, which can maintain turgor pressure and proper stomatal aperture which affects other physiological and biochemical processes (Wanget al., 2001). Osmotic regulation substances accumulated by desert shrubs mainly include inorganic ions such as K+, Na+, and Ca2+, and organic solutes consisting of proline, soluble sugar and glycinebetaine under environments with drought, high temperature and intense light. Main osmoregulation substances in plant tissues can be measured to represent its adaptive capability by osmoregulation (Zhao and Li, 1999).

In Minqin and Linze oasis-desert ecotone of Gansu Province, proline accumulation order isN. tangutorum＞C.mongolicum＞H. ammodendron, demonstrating that osmoregulation of proline inN. tangutorumis better (Shi, 2007).Abundant accumulation of proline may play an important role in drought adaptation inArtemisia sphaerocephalaandC. korshinskii, the proline concentration in whole plants were 1.8 to 25 times higher than those ofH. ammodendronandZ. xanthoxylonin the Alxa Desert of China(Zhanget al., 2004). The relationship between proline accumulation under stress, plant resistance and physiological role of proline in plant resistance should be considered with cell survival and protein metabolism (Zhouet al.,1999a). Soluble sugar accumulation is consistently taken as an adaptive mechanism for plants under water stress and content change can indicate stress degree. In hot summers,both soluble sugar and proline content in assimilating stems ofHalaxylon persicumshows a trend of quick accumulation, but the former was faster than the latter (Ruanet al., 2005). Soluble sugars and proline ofPeganum multisectumincreased with the aggravation of water stress,providing an inherent basis of drought tolerance and quick proline accumulation at the early stress stage, then dropping during the later stage when soluble sugars increased considerably, which indicates that the osmotic adjustment compensated each other (Liu and Zhao, 2005). Soluble sugar content ofT. ramosissimaandH. ammodendronat 55 °C were respectively 2 and 1.3 fold as those at 30 °C,showing that increasing heat stress resulted in plant dehydration and soluble sugar accumulation improved water-retaining capacity (Zhou ZBet al., 2005).Caragana stenophyllawith long-term adaptivity to an arid environment adjusted its cytoplasm osmotic potential mainly through accumulating soluble sugars and inorganic ions to accommodate an extremely harsh environment. This is probably an energy-saving adaptation strategy (Ma, 2004).However, the osmotic adjustment of desert shrubs is limited, especially under severe stress when osmotic regulation is reduced or even disappears (Wanget al., 2001;Zhang DYet al., 2003).

3.5. Anti-oxidation

The production and cleaning of activated oxygen free radicals in plants would be unbalanced under stress such as drought and high temperature, which results in the considerable accumulation of activated oxygen destroying lipids,proteins and other cellular components of plants. The intensification of lipid peroxidation is one of the main reasons for lipid damage (Zhouet al., 1999b). When the unsaturated bond of adipic acid in lipids is peroxidized,malondialdehyde (MDA) is produced. The content of MDA is an important parameter in representing the degree of lipid peroxidation and lipid damage by stress (Chen,1991; Wang, 1992). MDA of leaves ofZ. xanthoxylonaccumulated and relative permeability of the cell membrane increased under severe stress (3% soil water content), the MDA content and osmotic capability under soil water of 18%, 13% and 8% were all not significantly different from that of the control (Yang, 2004). This shows that the two-year oldZ.xanthoxylonpossessed high drought-tolerance and cell membrane was damaged only when exposed to severe drought stress. MDA content in leaves ofA. ordosicawas evidently lower than that ofH.scopariumpossibly due to the protection of water-storing tissue and thick cuticle inA. ordosica(Gaoet al., 2008).With increasing temperature, MDA content inC. caputmedusae,H. ammodendronandT. ramosissimatended to rise, but the increasing range was slight. Contrasted to MDA ofT. ramosissima,H. ammodendronandC. caputmedusaeat 30 °C, MDA at 50 °C only added to 1.2, 1.3 and 1.7 fold respectively, showing better resistance to lipid peroxidation (Zhou ZBet al., 2005).

Anti-oxidation systems which clean activated oxygen free radicals include the enzymatic defensive (anti-oxidation enzyme) and non-enzymatic defensive systems(antioxidant). Anti-oxidation enzymes consist mainly of SOD (superoxide dismutase), CAT (catalase), POD (peroxidase), and APX (ascorbate peroxidase) (Sergi and Lenonor, 2003). Anti-oxidation substances consist mainly of ASA (ascorbic acid), VE(DL-α-tocopherol), GSH (glutathione), CAR (carotene), ALK (alkaloid) and FLA (flavonoids) (Yinet al., 2007).

One of the products of superoxide anion dismutase reaction catalyzed by SOD is hydrogen peroxide (H2O2),which is active oxygen damaging to cell, so clearing of H2O2is key to removing active oxygen. H2O2is mainly eliminated by POD and CAT affecting with SOD to keep active oxygen at low levels. MDA content of eight species ofTamarixincreased under water stress, but they did not increase constantly with a descending process related to activity rise of SOD and POD (Wanget al., 2002).Caragana stenophyllahas higher POD and SOD activity,resulting in free radical and MDA content, and the permeability of the plasmamembrane was lower thanC. microphylla. This is an important characteristic ofC. stenophyllaadapting to an environment of drought, high temperature and intense light (Ma, 2004). SOD activity is positively correlated to resistance of plants to oxidation stress (Wanget al., 1989; Scandalios, 1993). SOD activity ofH. ammodendron,Z. xanthonylon,N. sphaerocarpa,S. passerina,N. tangutorum,C.stenophylla,C. mongolicum,A.sphaerocephala, andR. soongoricawere high under an arid environment, thus possessing better drought resistance(Gao, 2002). Activity of SOD, POD, CAT, and APX increased significantly at the early stage under medium and severe drought treatments. Activity of SOD and CAT increased significantly at the middle stage under medium drought treatment, and activity of SOD, POD and CAT increased at the late stage under medium stress (Hanet al.,2008). This suggests that under medium drought treatment the antioxidant enzyme and metabolites ofH. scopariumadjust to increase its antioxidant capability to alleviate or avoid active oxygen injury. At the initial stage of high temperature treatment, SOD activity ofC. caputmedusae,H. ammoendronandT. hohhenackeriincreased to the maximum and decreased quickly, suggesting that SOD activity of the three species could respond to adverse environments, and when the temperature raises to the range of 55 °C to 60 °C, lipid peroxidation would be exacerbated resulting in MDA increase and plant death (Zhou ZBet al.,2005).

ASA is one of the main antioxidants of plants which can reduce O2-, remove OH-, quench1O2, disproportionate H2O2, reproduce vitamin E and act jointly to decrease lipid peroxidation. The reduction of ASA content is often taken as an indicator demonstrating the decline of plant total anti-oxidation capability. GSH is a scavenger of H2O2preventing plant cell damage. CAR is an effective quencher of1O2, either directly or inhibiting the formation of1O2by quenching triplet chlorophyll (3Chl), thus eliminating damage of active oxygen to the photosynthetic apparatus(Yinet al., 2007). ASA content inC. mongolicumreached 1.6 times as that ofH. ammodendron, resulting in a lower O2-content. This shows that ASA content is correlated positively with anti-oxidation capability (Gonget al.,2004). ASA content inH. scopariumseedlings increased significantly at the early and middle stages under medium and severe drought stress and GSH content increased at middle and later periods under medium stress. ASA and GSH are possibly the main ways of removing H2O2in chlorophyll. GSH content inH. scopariumseedlings increased at initial and middle periods under medium and severe stress and decreased at the late stage, which shows that GSH can effectively reduce radical content and provide some protection for plant cells (Hanet al., 2008).GSH content was negatively correlated with H2O2content and acted as a main antioxidant removal of H2O2(Gonget al., 2004). Annual average content of beta carotene (β-Car)inC. stenophyllaunder extremely dry conditions was significantly higher than that under humid conditions acting as an anti-oxidant (Zhou HYet al., 2005).

4. Summary and prospect

As previously stated, mechanisms of desert shrubs adapting to an adverse environment include several levels from morphology to metabolism in many ways. Wickens(1998) classified the mechanisms of plants adapting to a drought environment into three kinds including drought-escape, drought-resistance and drought-tolerance.Drought-escape species adapt to a dry environment by quick growth and development (with a short life) or plasticity in developing stage, for instance, adjusting develop-ment period according to water status or transferring assimilates produced before flowering to seeds (redistribution) and completing the life history before severe water stress occurs. Drought-resistance plants adapt to an environment by forming xeromorphic structures or osmotic adjustment preventing water loss or enhancing water absorption or changing leaf morphology to avoid intense radiation. Drought-tolerant species can protect the photosynthetic apparatus and membrane structure stability to maintain metabolism through light respiration, thermal exhaustion or anti-oxidation mechanisms. Desert shrubs are perennials, so adapting a mechanism by quick individual development should not exist. Whether desert shrubs can transfer assimilates stored before flowering to reproduction organs or not has not been reported.

The adaptability of many desert shrubs to an adverse environment with drought, high temperature and strong light belong to drought-resistance and drought-tolerant types. Drought resistant shrubs possess morphological characteristics such as increasing stomatal and cuticle resistance, reducing radiation and leaf area, enlarging root density and depth, intensifying water conduction and physiological and biochemical features consisting of high water potential, high net photosynthetic rate, high water use efficiency and "midday depression" caused by stomatal factors. Drought-tolerant shrubs have morphological characteristics such as crystal or mucilage cells and physiological and biochemical traits including maintaining low potential, photo-inhibition caused by non-stomatal factors,accumulating considerable osmoregulation materials and possessing high anti-oxidation capability.

Many research findings have been achieved and the following characteristics can be summarized based on the aforementioned studies: (1) Researchers focused on the adaptivity of desert shrubs to water stress and the conclusions are complex, possibly due to different ways of forming water stress, and the criterion to divide water stress degree is not unified. In addition, the adaptivity of plants is related to the degree of water stress, stress time, plant development stage, genotype and factors resulting in water stress. (2) The aforementioned studies were not systematically researched, for example, they lacked a comprehensive adaptation strategy of desert shrubs to compound stress of drought, high temperature and excessive light, and adaptivity from the perspective of cells, organs, individuals and groups. In addition, the ecophysiological adaptation and gene regulation under compound stress have not been researched as a whole. Thus, future research on adaptation of desert shrubs to stress should be intensified from the following aspects: (1) Physiological and biochemical responding mechanisms of desert shrubs to compound stress from the perspective of cells, organs, individuals and groups should be researched; (2) The best conditions of light, temperature and maximal water use efficiency should be explored; (3) Studies should be carried out for biomass accumulation, gas exchange, water use efficiency, osmotic regulation, anti-oxidation mechanism and expression of drought-resistance genes to reveal comprehensively the relationship between desert shrubs and environmental factors combining molecular techniques.

This work was supported the National Key Technology R&D Program of China (No. 2007BAD46B03). The authors also want to express thanks to the editor and the anonymous reviewers for their valuable comments to the manuscript.

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10.3724/SP.J.1226.2011.00455

*Correspondence to: Prof. NianLai Chen, College of Resources and Environmental Sciences, Gansu Agricultural University,Lanzhou 730070, China. Tel: +86-931-7631741; Email: chennl@gsau.edu.cn

10 January 2011 Accepted: 14 July 2011