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Plant Acclimation and Adaptation toNatural and Anthropogenic Stress
M. N. V. PRASADa,b AND Z. RENGELc
bDepartment of Plant Sciences, University of Hyderabad, Hyderabad500046, IndiacSoil Science and Plant Nutrition, Faculty of Agriculture, TheUniversity of Western Australia, Nedlands, Perth WA 6907, Australia
Plant interaction with the environment and the vital underlying acclimation(short-term) and adaptation (long-term) strategies are topics of contemporaryinterest in the broad area of Stress of Life. Various environmental stress factorslimit plant productivity. Natural and anthropogenic changes in the environmentplay a crucial role in the productivity and survival as well as the general biologyof the plants. Eventually, stressed plants evolve mechanisms of endurance thatallow them to withstand these stress phenomena. Plants are vulnerable to variousstress factors such as light, UV-B radiation, high temperature, chilling and freez-ing, drought, flooding, ion stresses (salt and heavy metals), allelochemicals, her-bicides, polyamines, and air pollutants.
Supersaturated light in field conditions often causes photoinhibition of PS II,the multiprotein complex comprising D1, D2, cytochrome b559 and , two majorchlorophyll a proteins (CP47 and CP43), phosphoprotein (9 kDa), polypeptides ofthe oxygen evolving complex (33 kDa, 23 kDa, and 16kDa) and light-harvestingcomplex (LHC II), together with a number of low-molecular-weight polypeptidesranging from 3 to 7 kDa. One of the most prevalent acclimation mechanisms is thecapability of plants to dissipate excess excitation energy as heat. This phenome-non is accomplished through creation of a proton gradient across the thylakoidmembranes and formation of zeaxanthin. Phosphorylation of the LHC II complexalso serves to divert excess excitation energy away from PS II. Photoinhibited PSII centers are efficient quenchers of excitation energy and play a protective roleagainst photooxidative damage to the thylakoid membranes.1
UV-B induces certain high- and low-molecular-weight proteins that resembleheat-shockproduced proteins. Chloroplasts isolated from plants grown at differ-ent temperatures demonstrated variations in sensitivity when exposed to UV-B
aAdditional correspondence information: (Prasad) Fax: 91-040-3010145 or 3010120; e-mail: email@example.com
(Rengel) Fax: 61 8 9380 2557; e-mail: firstname.lastname@example.org
PRASAD & RENGEL: ACCLIMATION AND ADAPTATION 217
radiation. Chloroplasts from high-temperature grown plants showed greater sta-bility to UV-B than those from plants grown at ambient temperature. Thus, itappears that UV-B radiation mimics the response to heat shock, at least at theorganelle level. (See Kulandaivelu et al., 1997, in Ref. 2.)
CHILLING AND FREEZING
Several of the genes that are induced by chilling and freezing are also expressedin response to various other stresses involving water availability, salt, anddrought.3 Under chilling and freezing temperatures, a particular type of proteinscalled anti-freeze proteins (AFP) are synthesized and accumulated in the extracel-lular space during acclimation. These proteins bind to ice crystals in formation andrestrict their growth in the leaves of Secale cereale. Another type of protein, icenucleators, seem to be active in promoting heterogeneous ice nucleation. The com-bined effect of these proteins is thought (i) to promote extracellular ice formationat a much higher temperature than the theoretical ice nucleation point and (ii) torestrict crystal expansion. The genes encoding for a particular AFP have beencloned and expressed in transgenic plants. Although they seem to provide thetransgenic plants with the ability to minimize or prevent intracellular crystalliza-tion, it is still not clear whether this trait confers increased cold tolerance. Proteinspresent in the extracellular space of cold-acclimated leaves of winter rye seem toplay an essential role in freezing tolerance. (See Vezina et al., 1997, in Ref. 2.)
The stress-responsive polypeptides (70 and 23 kDa) are implicated in salt toler-ance of rice plants (Oryza sativa L.). However, the specific functions of these pro-teins need detailed study. In Mesembryanthemum crystallinum, proline accumulation(a rapid response on the cellular level) and crassulacean acid metabolism (CAM)induction (dependent on tissue organization) contribute to the salt resistance. Insalt-stressed M. crystallinum, various mRNAs encoding proteins of different bio-chemical pathways accumulated in leaf tissue. It was suggested that water stresstriggered the coordinated induction of mRNAs involved in different aspects of theadaptive stress response of the plants. Varied stressors, like drought or salinity,caused different transcription levels of several genes. Thus, the molecular stressresponse of M. crystallinum may be triggered by multiple signals. (See Hagemeyer,1997, in Ref. 2.)
FLOODING AND ANOXIA
Two genes, OS-ACS-1 and OS-ACS-3, are induced in rice plants subjected toflooding conditions. A third, ACC (1-aminocyclopropane-1-carboxylic acid) syn-thase gene OS-ACS-2, was also identified in rice, but its expression was repressedin response to low oxygen conditions. In addition to being induced by low oxygen
tensions, OS-ACS-1 and OS-ACS-3 are also induced by the indole-3-acetic acid(IAA), benzyladenine (BA), and LiCl treatments. The induction of these genes inresponse to low oxygen conditions was shown to be differential and tissue-specific;OS-ACS-1 is induced in the shoots, whereas OS-ACS-3 is induced in the roots.Induction of these genes is insensitive to protein synthesis inhibitors, suggestingthat they are the primary responses to the agent. (See Arteca, 1997, in Ref. 2.)
Accumulation of heat-shock proteins (Hsps) has been attributed to acquisitionof thermotolerance in plant systems. The Hsps have been detected in a number ofplant species. The Hsps have either high (80100 kDa, HMW-Hsps), intermediate(6873 kDa IMW-Hsps), or low molecular mass (1520 kDa, LMW-Hsps). Apartfrom heat shock, Hsps are also synthesized and accumulated in plants in responseto a large number of factors, such as arsenite, ethanol, heavy metals, water stress,abscisic acid, wounding, excess NaCl, chilling, and anoxic conditions. The major-ity of the Hsps are localized in cytoplasm and encoded by nuclear genes. (SeeSingla et al., 1997, in Ref. 2.)
Certain herbicides are known to generate active oxygen species by directinvolvement in radical production or by inhibition of biosynthetic pathways. Theantioxidative defense system that destroys active oxygen species generated dur-ing photosynthetic electron transport is not sufficient to protect the plant, andphotooxidative damages are increased. During photosynthesis the formation ofactive oxygen species is minimized by various regulatory mechanisms present inall plant cells, composed of both nonenzymic and enzymatic constituents. Thenonenzymatic antioxidants are hydrophilic antioxidants; ascorbate and glu-tathione, and lipophilic antioxidants -tocopherol and the carotenoid pigments.Phenolic and flavonoid compounds also scavenge superoxide, singlet oxygen, andhydroxyl radicals. More complex molecules such as phytic acid or phytoferritinform complexes with metals to prevent free-radical production by the Fe-cat-alyzed Haber-Weiss reaction.
Photosystem I electron acceptors mediate the transfer of electrons to O2, gen-erating toxic oxygen radicals that peroxidate the fatty acid side-chains of mem-brane lipids leading to loss of membrane integrity and causing a cascade ofoxidative reactions resulting in the inactivation of enzymes, lipid peroxidation,protein degradation, DNA strand breaks, and pigment bleaching. Application ofparaquat in two wheat cultivars induced photoinhibition and loss of fresh mass,protein, membrane integrity, and photosynthetic pigments, with Chl b decliningthe least and carotenoids declining the most. This is the only class of herbicidesinteracting with PS I that has been commercialized. (See Merlin, 1997, in Ref. 2.)
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The possible mechanisms conferring resistance to toxic metal ions include thefollowing: (1) physical avoidance of contaminated areas, (2) exudation of com-plexing agents into the rhizosphere, (3) binding in the cell wall, (4) afflux of metalions from the symplasm, (5) prevention of upward transport of metal ions intoabove-ground parts, (6) complexation with various ligands in the symplasm, (7)transport of metalligand complexes into vacuole, (8) storage of metal ions in thevacuole by complexation with vacuolar ligands, and (9) Formation of metal-resis-tant enzymes to minimize the internal injury caused by toxicity.4 (Also see Prasad,1997, in Ref. 2).
Many of the allelochemicals are known to modify either the synthesis or activ-ity of various enzymes in vitro and in vivo. The activity of glucose-6-phosphatedehydrogenase was inhibited with ferulic acid and other phenolic compounds.Often most of the allelochemicals are shown to exert a dual effect in regulating theenzyme activities; that is, low concentrations tend to activate, whereas high con-centrations inhibit the enzyme activity. Increase in activity of some of the oxida-tive enzymes (peroxidase, catalase, indole acetic acid oxidase) has been observedin ferulic acidtreated maize seedlings,5 together with a considerable rise inphenylpropanoid enzymes such as phenylalanine ammonialyase and cinnamylal-cohol dehydrogenase, thus activating oxidative and phenylpropanoid metabo-lisms. Further, under most of the allelopathic situations, a decrease in the activitiesof nitrogen-fixing enzymes such as nitrate reductase has been observed. In maize,the inhibitory nature of ferulic acid to hydrolytic enzymes, that is, amylase, mal-tase, invertase, protease, and acid phosphatase of maize seeds, which are involvedin the mobilization of reserve food material and ascribed these changes to growthinhibition.6 (See also Devi et al. 1997 in Ref. 2.)
Several investigations have emphasized the many and varied roles ofpolyamines and associated enzymes in molecular, cellular, and physiological func-tions such as regulation of nucleic acid synthesis and function, protein synthesis,cell growth and differentiation, embryo development, physical and chemicalproperties of membranes, hormones, and modulation of enzyme activities. Therole of polyamines in many cellular and molecular processes has also beendemonstrated. For instance, polyamines have been shown to stimulate phospho-rylation of protein kinase. Certain soluble and plasma membrane proteinsincrease rates of RNA and protein synthesis and initiate DNA synthesis. Existenceof posttranslational modification of polyamine-bound polypeptides has beenreported. Polyamines also polymerize Rubisco subunits and bind to some light-harvesting complex proteins. Polyamines, especially Put, have been known toaccumulate in plants under stress conditions. The specific inhibition of fungalpolyamine biosynthesis has also been proved as a new method of protectinghigher plants from phytopathogenic fungi. (See Rajam, 1997, in Ref. 2.)
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The oxidative stress results from deleterious effects of reduced oxygen speciessuch as superoxide and hydrogen peroxide. These oxygen species can formhydroxyl radicals (OH), the most reactive species known to chemistry.7 Hydroxylradicals cause lipid peroxidation, protein denaturation, DNA mutation, photo-synthesis inhibition, and so forth. Under physiological conditions, plants producesignificant amounts of superoxide and hydrogen peroxide, for example, in theelectron transport that occurs during photosynthetic reactions or during ATP gen-eration in mitochondria, and in the process of -oxidation of fatty acids in gly-oxysomes. In order to survive, aerobic organisms have evolved a defensemechanism against oxidative stress. Because hydroxyl radicals are far too reactiveto be controlled easily, the defense mechanism is based on elimination of super-oxide and hydrogen peroxide.
The central role in the plant antioxidative mechanism is played by superoxidedismutase (SOD, EC 18.104.22.168), an enzyme that converts superoxide into hydrogenperoxide, which is then broken down by either catalase (EC 22.214.171.124) or variousperoxidases. The most important peroxidase-type enzymes are ascorbate peroxi-dase (APX, EC 126.96.36.199), glutathione reductase (GR, EC 188.8.131.52), guaiacol peroxi-dase (GP, EC 184.108.40.206), and dehydroascorbate reductase (DHAR).7 Somenon-enzymatic components, like ascorbic acid and glutathione, are also importantcomponents of the antioxidative system.7,8
A number of reports have shown that environmental stresses are at least partlycaused by the oxidative stress due to an increase in production of superoxide rad-icals and hydrogen peroxide. Such oxidative damage has been reported for highlight intensity,9,10 herbicide exposure,11 ozone and SO2,
12 cold,7 drought,7,13,14 flood-ing (Arteca, 1997, in Ref. 2), salt toxicity,15 heavy metal toxicity,16,17 and deficiencyof essential elements.9,18,19
There is a significant difference in tolerance to oxidative stress among geno-types of crop species differing in tolerance to environmental stresses. Salt-resis-tant cultivars of pea,15 waterlogging-resistant genotypes of iris, ozone-resistantvarieties of tobacco, and chilling-resistant genotypes of maize,7 all showed greateractivity of SOD and lower levels of free oxygen radicals compared to the sensitivegenotypes exposed to the same level of stress. These results indicate thatincreased activity of antioxidant enzymes is an important part of the plantsresponse to various environmental stresses.
Genes coding for various antioxidant enzymes have been cloned and success-fully used to transform model plants to study the role of antioxidant enzymes invarious environmental stresses.7 The SOD genes were cloned from Arabidopsis,spinach, pea, soybean, tobacco, tomato, petunia, and maize7,20; the list of plantspecies successfully transformed with the SOD genes includes tobacco, cotton,lucerne, and potato.7 Overexpression of the SOD genes generally leads toincreased biosynthesis of SOD and increased resistance of plants to the oxidativestress induced by a range of environmental stimuli. In addition, the APX geneshave been cloned from Arabidopsis and pea; transgenic tobacco plants overex-pressing the APX genes are more tolerant to oxidative stress.21
Although it is clear that overexpression of the SOD genes leads to increasedresistance to the oxidative damage caused by environmental stresses, it appearsthat type and localization of SOD are important factors determining the level ofprotection from oxidative damage.7 The reason for this observation is thatCu/Zn-SOD is inhibited by increased levels of hydrogen peroxide, which is a
220 ANNALS NEW YORK ACADEMY OF SCIENCES
final product of the enzymatic reaction controlled by SOD. Therefore, a simulta-neous increase in activity of APX is required to ensure a quick breakdown ofhydrogen peroxide before it accumulates at the levels that are inhibitory to SOD.The successful targeting of APX to chloroplasts in transformed plants hasrecently been achieved. An alternative way of ensuring that overexpression ofSOD genes confers increased resistance to environmental stresses is to targetH2O2-resistant Mn-SOD to the chloroplast stroma. Plants transformed with thischimeric gene overexpressed Mn-SOD that was correctly targeted to chloro-plasts; these plants showed increased resistance to environmental stresses.7
Although the effects of overexpression of single genes are generally small, it isto be expected that in plants, exposed to frequent periods of mild or moderate lev-els of various environmental stresses during the growing period, even smallincreases in resistance to these stresses, conferred by increased expression ofantioxidative enzymes, could be additive and thus have a substantial effect on pre-venting growth reductions.
Abscisic acid (ABA) seems to be the panacea for plant stress. It is playing a keyrole in co-stress manifestations in the conversion of stressful environmental sig-nals to gene expression.22 Thus, involvement of ABA in plant stress is emerging asa priority area of research (FIG. 1).
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FIGURE 1. ABA involvement in co-stress manifestations. Conclusive evidence exists forthe following stresses chilling and freezing (Vezina et al., 1997, in Ref. 2); drought (Freitas,1997, in Ref. 2); salinity (Hagemeyer in Ref. 2); flooding and anoxia (Arteca, 1997, in Ref. 2);tolerance to metal ions23,24; and fungal disease resistance (Black, 1991, in Ref. 3).
MNVP is thankful to the University of Hyderabad (University GrantsCommission, New Delhi, unassigned grant) and Council of Scientific andIndustrial Research, New Delhi for a partial travel grant enabling me to chair aworkshop at the Stress of Life Congress.
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