YaJuan Zhu, Lei Li, ZhiQing Jia

Institute of Desertification Studies, Chinese Academy of Forestry, Beijing 100091, China

Research advances on drought resistance mechanism of plant species in arid zones of China

YaJuan Zhu, Lei Li, ZhiQing Jia*

Institute of Desertification Studies, Chinese Academy of Forestry, Beijing 100091, China

Drought and shortage of water resources, which restrict the economy, society development and environmental protection, are key factors in arid zones of China. In the arid zones of Western China, researching plant drought resistance mechanism, selecting plant species with higher drought resistance, and developing water-saving techniques, are important for environmental improvement and economic development. This paper reviews research advances on drought resistance mechanism of plant species, based on research of morphological, physiological, and ecological adaptation mechanism of plant species under drought stress, such as anatomical structure of root systems and leaves, photosynthesis, antioxidant enzyme system,malondialdehyde (MDA), osmotic adjustment, endogenous hormone, drought-induced proteins and δ13C. Finally, this paper points out the key field of future research.

arid zone; drought resistance; drought resistance mechanism; evaluated index

1. Introduction

One third of the total land of China is located in an arid zone. Drought and the shortage of water resources, which restrict the economy, society development and ecological environmental protection, are key factors that affect the development of the western regions (Feng and Jiang, 2001).Because of some natural factors (such as decreasing rainfall and increasing drought) and some artificial factors (such as population increase and irrational exploitation), severe desertification has occurred in portions of the arid zones. Land desertification has become one of the most serious environmental problems to which people from all over the world are paying attention. Some effective ways that could prevent and reduce desertification are restoring degraded ecosystems through use of biological and engineering methods (Yan,2005). Plant species play an important role in building forest shelter belt and sand-fixing system, including trees, shrubs and herbaceous plants. Therefore, researching plant drought resistance mechanism, selecting drought-resistant plant species, and enhancing water-saving techniques of transplant,are important for desertification control and other environmental improvements in arid zones of China.

Under drought stress, a series of physiological and biochemical changes occur in plants and these changes may affect the growth and development of plants. Research on plant physiology of drought resistance is useful in understanding the response and adaptation of plants to drought stress, to find interspecific differences, and provide theoretical evidence for drought-resistance identification of plant species. At present, there have been numerous studies on selecting cultivars with superior traits, especially crops and trees, but few studies have been done in an extreme arid environment. There are two main methods used when studying drought resistance of plants. One method examines the relationship between morphological structure and drought resistance, including leaf anatomical structure and biomass. Another method explains the indicative function of plant physiological and biochemical indices on drought resistance (Huanget al., 1997). These physiological indices include such factors as water physiology index (e.g., water potential), photosynthetic characteristics, enzyme activity,protoplasm character, osmotic adjustment and endogenous hormones (He, 2005). In recent years, stable carbon isotope technology is used to indirectly measure long term water use efficiency of C3plants and compare their drought resistance(Yanget al., 2007).

2. The adaptation of plants to drought stress and their classification

In view of water physiological characteristics, plants with drought resistance mechanism of high water potential can delay dehydration mainly from restricting water loss or absorbing water, thus keeping a high water potential of tissue under drought stress. Plants with low water potential drought resistance mechanism not only have the ability of absorbing water and lessening water lose, but also have a strong tolerance of dehydration, which is mainly expressed as a lower basic osmotic potential, available solute accumulation (decreasing their osmotic potential) and protoplasm resistance. Osmotic adjustment and turgor maintenance are important ways of resisting drought during a low water potential circumstance (Larcher, 1980).

In view of life history, the adaptation to water shortage and drought resistance mechanism of xerophytes is the relationship characteristic between organisms and the environment. Every xerophyte has a complex survival mechanism which insures its survival and development in a specific arid environment. There are numerous classification types of xerophytes and they can be divide into three categories according to comprehensive physiological indices: (1) drought evasion, these plants have a short growth cycle and complete life cycle before the beginning of the dry season,e.g.ephemeral plants. (2) drought avoidance, these plants restrict water consumption and/or develop a vast root system to avoid being killed by drought. They often maintain high and stable transpiration and photosynthetic rates, such as deep-rooted desert shrubs. (3) drought endurance, these plants can survive without available water for a long period of time, depend on water in storage tissues,e.g. cactus(Denget al., 2008).

3. Research advances on drought resistant mechanism of plants

In arid zones, especially in deserts, plants grow in a dry and hot environment and have developed unique adaptive characteristics in morphological structure and physiological functions. Many studies have been done in relation to the adaptation of desert plants to the environment (Jiang and Zhu, 2001). Drought resistance of plants is a kind of functional adaptation to stress. The drought resistance mechanism is not the function of one factor, but the synthesis of many characteristics which mainly relate to morphological,structural and physiological characteristics. According to recent research, they mainly include aspects listed below.

3.1. Morphological adaptation characteristic and drought resistance

The root system of some desert woody plants is strong and deep, with a high root/shoot ratio, thus it can absorb and use soil water efficiently, especially water in deep soil layers.Some plants have small leaf cells with thick cell walls,strong mechanical tissue, numerous small stoma, dense leaf venation, strong conductive tissue, much tomentum on leaf surface, and high degree of cutinization or thick wax. These morphological and structural characteristics could increase water absorbability and transportation in plants, or decrease water loss, thus enhancing drought resistance (Zhang JS,2006). For example, the study of morphological and anatomical characteristics ofAmmopiptanthus mongolicusindicates that it can resist drought and increase water use efficiency (Zhouet al., 2001). The comparison of some xeric structures ofXanthoceras sorbifolia,Hippophae rhamnoides,andOstryopsis davidiana, such as cuticle, palisade, main venation, mesophyll thickness, cell concentration of the first layer of palisade cells, and side vascular bundle density,indicates that two of the three plants have a drought resistant structure whereas all three have drought-resistant characteristics, respectively. According to these indices, the sequence of drought resistance wasX. sorbifolia＞H. rhamnoides＞O.davidiana(Wang, 2003). A study of nine trees (such asLaburnum alpinum,Caragana korshinskiiandLycium barbarum) found that leaves with higher drought resistance had some anatomical characteristics, such as higher cell concentration, strong palisade tissue (2-3 layers), greater ratio of palisade/mesophyll cells, and thicker upper epidermis, lower epidermis and cuticle (Fan, 2005). The most typical drought resistant indices of six shrubs, includingC. korshinskii, were cell layer thickness of upper cuticle, palisade thickness and stomata density (Hanet al., 2006). Therefore, leaf anatomical structure is a key index for the study of drought resistance of plant species.

3.2. Photosynthetic physiological index and drought resistance

Previous studies in China and other countries have indicated that photosynthesis is restricted and photosynthetic rates decreased in drought conditions. The general opinion is that plant species with higher drought resistance can maintain a relatively high photosynthetic rate or net photosynthetic rate, and photosynthetic rate is a reliable index for the identification of drought resistance (Hu and Wang, 1998).For example, the photosynthetic rates ofReaumuria soongorica,Salsola passerina,Caragana korshinskiiandArtemisia ordosicadecreased as drought levels increased in gradual soil drought (Songet al., 2008). The net photosynthetic rate, stomata conductivity and stomata limitation value ofA. mongolicusdecreased with an increase of air tempera-ture (Li and Feng, 1999). The main reason for the decrease of photosynthetic rate ofCalligonum mongolicumwas water shortage in drought conditions (Suet al., 2003b). The net photosynthetic rate ofCalligonum arborescensshowed a single peak curve in different growing seasons and in different treatments, and its photosynthesis was significantly inhibited by drought stress (Yanet al., 2007). The trend of stomata conductance and photosynthetic rate ofGlycyrrhiza uralensiswas consistent with an increase of drought stress(Liu CLet al., 2006).

Stomata conductance (gs) determines the absorbability of CO2in photosynthesis and water emission in transpiration. It is sensitive to change of environmental factors and can be affected by all kinds of factors which influence plant photosynthesis and leaf water status (Wang and Zhou, 2000). ThegsofTamarix ramosissimawas significantly related to water use efficiency (WUE) in different months (Denget al.,2003). The daily change ofgsofPopulus euphraticashowed a periodic fluctuation curve, and its net photosynthetic rate and transpiration rate also showed a similar trend (Siet al.,2008).

Water use efficiency (WUE) of plants is the comprehensive reflection of photosynthesis and transpiration. This efficiency is expressed as the ratio of net photosynthetic rate and transpiration rate. Plants with higher WUE can use water economically and has a higher drought resistance (Bierhuizen and Slatyer, 1965). For example, the study ofMedicago sativaillustrated that WUE can reflect the adaptive ability of plants to stress (Liu YHet al., 2006).

3.3. Oxidation enzyme activity and drought resistance

The damage of drought to plants is related to the accumulation of active oxygen in plants resulting in membrane peroxidation and then leads to a membrane damage. Active oxygen can destroy much of the molecular biological function, including membrane peroxidation. However, the organism has developed complete and complex enzyme and non-enzyme antioxidation protective systems to eliminate active oxygen. There are two kinds of antioxidation systems in plants: (1) enzyme protective systems, such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT); (2)non-enzyme protective systems, such as ascorbic acid(ASA), glutathione (GSH), cytochrome f (Cytf), vitamin E and carotenoid (Panet al., 2004).

SOD, CAT and POD are protective enzymes in organisms and play an important role in eliminating free radicals.SOD can convert O2-into H2O2, and CAT and POD can eliminate H2O2producing H2O. These three enzymes cooperate with each other and keep radicals at a low level, thus prevent membrane damage and protect the cells. There is a difference in the activity of SOD, CAT and POD in different plant genotypes. The genotype activity of SOD, POD and CAT with higher drought resistance was higher in drought stress and thus can effectively eliminate active oxygen, preventing membrane peroxidation (Jiet al., 2006). SOD activity of drought resistant plants generally increase and the elimination ability of active oxygen also increases in suitable conditions. The change of CAT and POD often show similar trends (Zhang JS, 2006). Drought resistant ability of trees is in close relationship with damage level and activity change of protective enzymes in drought stress (Sunet al., 2003).For example, the study of four desert plants,R. soongorica,Haloxylon ammodendron,Limonium gmeliniiandAlhagi sparsifolia, indicates that SOD content of shrubs was higher than herbaceous plants in drought stress (Chen Tet al.,2002). In ten desert plants,S. passerina,Nitraria sphaerocarpa,Nitraria tangutorum,H. ammodendron,Zygophyllum xanthonylon,R. soongorica,C. mongolicum,Caragana stenophylla,Caragana sinicaandArtemisia sphaerocephala,plants growing in arid environments have higher SOD activity and stronger drought resistance (Gao, 2002). The response of three desert plants to drought stress shows that SOD activity ofC. mongolicumwas significantly higher thanH. ammodendronandElaeagnus angustifolia, and this was consistent with its low content of O2-(Gonget al.,2004). In other words, SOD activity of plants is in close relation with its drought resistance.

3.4. MDA and drought resistance

MDA (malonaldehyde) is one of the main products of membrane peroxidation, and it is poisonous to cells which can induce functional turbulence of cell membranes. The change of MDA content reflects the degree of membrane peroxidation caused by the communication of oxygen radicals in environmental stress, and the degree of change of membrane peroxidation reflects damage level of plant cells(Zhaoet al., 2004). MDA content decreases with an increase of soil water content, and the decrease extent is higher in plant varieties with higher drought resistance. MDA is used as a peroxidation index of membrane lipids and indicates peroxidation level of cell membrane lipids and the response of plants to drought stress (Ruet al., 2006). For example,leaf MDA mole concentrations of three varieties ofRobinia psuedoacaciaincreased in gradual progress of soil drought,and this indicates that peroxidation of membrane lipids was induced by water stress (Zhanget al., 2005). MDA content of dry leaves ofH. rhamnoidesgradually increased as time extended; MDA content increased slightly in low and moderate drought; MDA content in serious drought increased significantly. Leaves ofH. rhamnoideswere affected by a serious quick drought, indicating that it was damaged by severe, long term drought (Wang, 2006).

3.5. Osmotic adjustment and drought resistance of plants

The mechanism of osmotic adjustment is always a key aspect in drought resistance studies. There are three explanations about osmotic adjustment mechanism: (1) Osmotic adjustment material acts as a kind of osmotic pressure agent,stabilizing the balance of osmotic pressure and enhancing the water conservation ability of plants. (2) Osmotic adjustment material acts as a solvent, replacing water and participating in biochemical reactions, and is a low molecular weight partner in this circumstance. (3) Osmotic adjustment material combines with the hydrophobic surface of proteins and transfers it to the hydrophilic surface, increasing the combination of water molecules with the previous hydrophilic region, stabilizing the hydrophilic surface and ensuring the stabilization of protein structures (Jiet al., 2006).

Plants maintain particular turgidity by osmotic adjustment in drought conditions and prevent hydration, increase the growth of root systems, enhance water absorption, and thus provide cell growth and normal physiological progress.The key to osmotic adjustment is the initiative accumulation of solutes in drought conditions. The materials which participate in osmotic adjustment include inorganic ions (e.g.,K+, Na+, Cl-, Ca2+, Mg2+) and organic matter (e.g., soluble sugar, proline, betaine, sorbierite and mannitol). There are numerous studies about proline in osmotic adjustment material. Free proline content in plants is low in regular conditions; however, free proline will accumulate abundantly in drought, low temperature and salt stress. Proline may increase dozens, even hundreds of times than the original amount in drought stress (Liuet al., 2002). More proline accumulates in plants in drier soils; in the same soil moisture,more proline accumulates in plants with higher drought resistance. Free proline content can be used in breeding and identifying the drought resistance of crops as a physiological index of drought resistance. More proline accumulates in varieties with more drought resistance, and this index has been used in study of drought resistance about 12 species ofCaraganaspp. (Zhanget al., 2006) and 4 plants in Lanzhou,includingC. korshinskii,E. angustifolia,A. mongolicusandR. pseudoacacia(Jianget al., 2006).

3.6. Hormone, stomata adjustment and drought resistance

The endogenous hormone is a regular part of the biochemical process of plants. The mechanism of stomatal closure induced by drought stress has been a controversial question for some time. The most acceptable viewpoint is that ABA (abscisic acid) content is increased by water stress and is a trigger to stimulate stomata closer (Jiet al., 2006). It was proven that exogenous ABA can inhibit the re-opening of closed stomata, and cause the opened stomata to close again (Liu and Zhang, 1994). It was found in previous studies that ABA synthesized in roots under drought stress can act as the chemical "information" material. Their antagonism and allocation balance in underground and above ground parts can affect stomata behavior, photosynthesis and morphogenesis, and increase the use efficiency of water and assimilation products. Therefore, plants can normally grow in arid environments (Daviset al., 1986; Zhang and Davis,1989).

The potential effect of hormones was confirmed in the adaptation of plants to drought. ABA content in plants increased in arid environments and made plants resistant to unfavorable environments. ABA can regulate the opening and closure of stomata and promote the absorption of water and ions in root systems. For example, ABA accumulation inP. euphraticais a unique way to resist drought, decrease its growth rate, promote the accumulation of assimilation products, increase water retaining capacity, and enhance the adaptation ability to arid environments. ABA content inP.euphraticachanged regularly with the variation of ground water table in arid environments in the lower reaches of Tarim River. It was found that there is a close relationship between ABA accumulation and drought resistance inP.euphratica(Chen YPet al., 2004). ABA content increased significantly inH. rhamnoidesleaves with the decrease of soil water content, and female plants are superior to male plants (Liuet al., 2005). ABA content has a maximum value in all endogenous hormones ofPotaninia mongolica, and the accumulation of ABA regulated the adaptation ofP.mongolicato arid environments (Houet al., 2005). There are fewer reports about the effects of hormones onH. ammodendron, such as ABA. ABA content inH. ammodendronwas increased by drought (Jianget al., 2001; Guoet al.,2004).

3.7. Drought induced proteins and drought resistance

The synthesis of some proteins in plants is inhibited by drought stress, total protein synthesis rate decreased, and some new drought induced proteins are synthesized simultaneously. Drought induced proteins can protect plants in the progressive adaptation to stress and enhance stress resistance of plants to drought. The study of drought induced proteins has made advances with the further development of the theory and technology of molecular biology. Some genes that encode drought induced proteins and protein kinase genes relevant to stress resistance have been separated and sequenced. Before the occurrence of all kinds of damage caused by water deficits, plants respond to water stress by adaptive regulation, including gene expression, and this is the protective selection of plants itself (Zhang and Zhu,2004). Drought induced proteins can be divided into two categories according to its functions: (1) functional protein,plays a protective role in the cell directly, such as LEA protein, osmotic adjustment protein, aquaporin, and metabolic enzymes; (2) regulatory protein, participates in signal transduction of water stress or gene expression regulation, plays a protective role indirectly, including protein kinase, phospholipase C, phospholipase D, G protein, calmodulin, transfer factors and some signal factors. For example, the soluble protein content of the seedling ofPinus koraiensisandBetula platyphylladecreased with the reduction of soil water content, which might be due to the performance of damage caused by water stress (Yan and Li, 1999; Sunet al., 2001).This result is similar to the study aboutSophora viciifolia(Wanget al., 2005). However, there is a difference of soluble protein content in different trees and the drought resis-tance could not be estimated only by protein content. Protein content changes in water stress conditions and protein composition changes simultaneously. The qualitative change might play a more important role in drought resistance. This is the preliminary cognition about the role of drought induced proteins in woody plants, which still need further study.

3.8. Stable carbon isotope and drought resistance

There is carbon isotope discrimination in photosynthesis.Leaves prefers to assimilate12CO2whereas reject13CO2,resulting in lower levels of13C in leaves than air CO2. This phenomenon is obvious when leaf stomata are completely open (Chen SPet al., 2004), which is the basis for the use of carbon isotope technology in plant ecology (Chen SPet al.,2002). The value of plant carbon isotope partly depends on innate CO2concentration or stomata conductance and photosynthetic rate. Leaf carbon isotope composition (δ13C value) is an integrative index ofCi/Caratio. From another point of view, it can be used to indicate the long term water use efficiency of C3plants and reflects the ecophysiological characteristics in total growing season (Liu and Li, 2008).

The increase of leaf δ13C values is a result of drought(Chen SPet al., 2002). Leaf stomatal conductance decreased and then innate CO2concentration was reduced by drought.C3plants with higher δ13C values have higher water use efficiency (WUE), which contributes to the adaptation to drought. Leaf δ13C values of C3plants can indicate long term WUE as an index about long term ecophysiological processes (Chen SPet al., 2002; Liuet al., 2008). A study on the same species or species in the same genus in Fukang (Xinjiang Uygur Autonomous Region) and Jinta (Gansu Province) indicate that one of the superiority of δ13C values was to estimate total WUE of leaves or plant growth by analyzing carbon metabolin accumulated in leaves for a long period, and its examination was not restricted by time or season. Leaf δ13C values decreased by 0.010‰-0.015‰ when annual mean precipitation increased by 1 mm. The reliability of WUE indicated by leaf δ13C values is explained indirectly by this regularity (Chen Tet al., 2002). Leaf δ13C values ofR. soongoricaincreased with the decrease of soil water content (Maet al., 2005, 2007). The WUE of different C3plants can be estimated by comparing their δ13C values. For example, the δ13C value ofC. korshinskiiis higher thanA. ordosica, which indicates that WUE ofC. korshinskiiis higher thanA. ordosica(Zhaoet al., 2005).

Factors that affect plant δ13C values include season, climate and latitude. Plant δ13C values and water use efficiency indicated by δ13C values changed in different seasons. For example, water use efficiency of some desert plants was different in different seasons in central region of Hexi Corridor, includingC. korshinskiiandN. sphaerocarpa. The total tendency was higher WUE in early growing season and lower WUE in late growing season (Suet al., 2003a). δ13C values in leaves of different desert plants was different in different growing seasons. Leaf δ13C values ofC. korshiskii,N. sphaerocarpaandHedysarum scopariumvaried from-25‰ to -28‰ (Suet al., 2005). Plant δ13C values are also affected by habitat and climate. For example, δ13C values and WUE ofCarex korshinskiiincreased significantly with the decrease of available soil water (Chen SPet al., 2004).

4. Study trends about plant drought resistance

The study about drought resistance mechanism and the change of ecophysiological and biochemical indices are important in finding the simple index of drought resistance,breeding, and the choice of plants with higher drought resistance. Drought resistant performance of ecology, anatomy,morphology and physiology has been intensely studied from the viewpoint of organs, individuals, populations and other levels until now. Some indices were proposed to evaluate drought resistance, and the cognition of plant drought resistance was successfully discussed by these studies (Zhang YB, 2006). The adaptation to drought is various in different plants, and some plants may have many mechanisms to resist drought. The physiological index is widely used in experiments, such as photosynthesis. However, water use efficiency measured by photosynthetic instruments and other physiological indices only indicates instantaneous behavior of leaves. These indices change momentarily with the change of season and environmental conditions. Therefore, a simple and feasible index must be found to evaluate long term water use efficiency in plant growth processes. Recently, leaf δ13C values are generally used as a reliable index of long term water use efficiency. One of its superiority is estimating total WUE of leaves or plant growth by analyzing long term carbon metabolin accumulation in leaves, and its examination is not restricted by time or season. After the sample is collected and dried, it can be kept and measured when convenient (Chen SPet al., 2002). Although the existence, structure and gene express pattern of drought induced proteins are thoroughly comprehended, the function and express mechanism of most drought induced proteins are still unclear. The intensive study of drought induced proteins can not only provide an understanding of stress resistance mechanism from a molecular level, but also from the foundation of crop improvement by use of gene engineering technology. In the future, with a deep understanding of drought induced proteins, tremendous progress can be achieved in the physiological and biochemical mechanism of drought resistance and the breeding of drought resistant variations (Zhang and Zhu, 2004).

The sufficient use of plant resources, especially psammophyte and xerophytic resources of China, the study of physiological mechanism of drought resistance, and the enhancement of drought resistance of plants are important to mitigate and prevent desertification, and protect the environment, both in theory and practice. The key to future studies is to clarify systematically the material basis and physiological functions of drought resistance from multiple levels, using leaf δ13C values in many study areas of plant ecology as a reliable index that indicate long term water use efficiency of C3plants, and enhancing the study of drought resistant plants integrated with drought induced proteins and gene engineering technology.

Acknowledgment:

This study was supported by the Key Project of Research Institute of Forestry, Chinese Academy of Forestry(ZD200908) and the National Eleventh "Five-year Plan"Science and Technology Funded Project of the State Forestry Administration, P. R. of China (2006BAD26B0101).The authors thank comments by two anonymous reviewers.

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10.3724/SP.J.1226.2011.00448

*Correspondence to: ZhiQing Jia, Professor of Institute of Desertification Studies, Chinese Academy of Forestry, Beijing 100091,China. Email: jiazq@caf.ac.cn

12 May 2011 Accepted: 16 August 2011