differential responses in growth, physiological processes ... papers/jtas vol...differential...

Pertanika J. Trop. Agric. Sci. 27(1): 47-55 (2004) ISSN: 1511-3701© Universiti Putra Malaysia Press

Differential Responses in Growth, Physiological Processes and PeroxidaseActivity of Young Mango (Mangifera indica) and Citrus

(Citrus sinensis L) Plants to Water Deficit

'MOHD RAZI ISMAIL, 2ABD GHANI MUHAMMAD & 'ISMAIL IBERAHIM'Department of Crop Science

Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia2MARDI Research Station Jeram Pasu, 16800 Pasir Putih, Kelantan

Keywords: Water deficits, mango ( Mangifera indica), citrus (Citrus sinensis), water relations, stomatalconductance, peroxidase activity

ABSTRAK

Pengaruh tegasan air terhadap pertumbuhan, proses fisiologi, aktiviti prolina dan peroksida telah dikaji padatanaman mangga (Mangifera indica) dan limau (Citrus sinensis,) didalam rumah tanaman. Dalam keadaanpengurangan air secara berperingkat, pokok mangga dan limau menunjukkan perbezaan dalam potensi air,konduksi stomata, perkembangan daun dan aktiviti peroksida. Perubahan stomata tidak bergantung padaperubahan potensi air daun pada kedua-dua tanaman apabila tegasan air berlangsung. Pengurangan konduksistomata pada pokok mangga adalah lebih tinggi dibandingkan dengan limau, menunjukkan bahawa limauberupaya mengaxval kehilangan air terhadap perubahan kedapataan air. Aktiviti peroksida menunjukkanpeningkatan bererti dalam keadaan pengurangan air tanah bagi tanaman limau. Terdapat peningkatan diantara 6 hingga 10 kali ganda kandungan prolina bagi tanaman mangga dan limau apabila pokokdidedahkan kepada tegasan air. Peningkatan prolina yang ketara bagi tanaman limau berbanding manggamenunjukkan ketahanan tegasan air yang tinggi tanaman limau berbanding mangga. Bukti ini diperkukuhkandengan pemulihan semula yang cepat selepas pemberian air kepada pokok limau dibandingkan pokok manggamelibatkan regenerasi pucuk baru yang cepat.

ABSTRACT

The effects of water deficit on growth, plant physiological processes and peroxidase activity were studied for youngmango (Mangifera indica) and citrus (Citrus sinensis L) plants in the greenhouse. Under gradually decreasingsoil moisture content, mango and citrus differed in their leaf water potential, stomatal conductance, leaf growthand peroxidase activity. Stomata of both plants responded independently to the changes in leaf water potential assoil drying progressed. The reduction in stomatal conductance in mango xoas greater than citrus suggesting thatcitrus was able to control zvater loss better than mango to the changing condition of water availability in the rootzone. Peroxidase activity increased significantly in water stressed citrus plants. There was a 6-10 fold increase inproline content when both species were exposed to water stress. Citrus plants accumulated higher proline levelssuggesting that they can tolerate water stress compared to mango. This was also evident by a faster recovery afterrewatering in citrus compared to mango plants that involved regeneration of new shoots.

INTRODUCTION

Water deficit is one of the environmentallylimiting factors for fruit tree establishment inthe field from the nursery. Roots of young fruittrees are often not fully developed attransplanting so a small degree of water deficitcan cause plant water stress and mortality.Although Malaysia is tropical and characterizedby adequate sources of water, the incidence of

water shortage occurs from time to time in someof the agricultural production areas. Theproblem of plant mortality is often serious inconditions where cultivation is to be done inundulating areas where there are difficulties ininstalling a proper irrigation system.

Plants usually developed physiologicalresponses as well as ecological strategies to copewith water stress. These responses allow them to

MOHD RAZI ISMAIL, ABD GHANI MUHAMMAD & ISMAIL IBERAHIM

survive and to sustain some growth under adverseconditions. Plants' responses depend on thespecies differences, nature of water shortageinducing physiological responses to short termchanges, acclimation to a certain level of wateravailability and adaptation to drought (Jones1983; Ruiz-Sanchev et al 2000). Plant adaptabilityto localized water deficit has been attributedmainly to maintenance of water status by utilizingavailable soil and by chemical signaling. Variousmetabolites and chemicals have been observedto accumulate in plant tissues during water andsalt stress and contribute to osmotic adjustment.Some species that adapt to mild and/or moderatedrought stress exhibit increases in activities ofantioxidant enzymes such as super oxidedismutase, catalase and peroxidase (Fu andHuang 2001). Although the concentration ofsome amino acids increase during water stress,there is general agreement that prolineconcentration is profound (Kohl et al. 1991;Albernethy et al 1998). The information gatheredon drought resistance mechanism makes it easierto plan for crop zoning based on the wateravailability and to designed irrigation strategiesfor optimizing water used.

Mango and citrus are two of the fifteen fruitspecies that had been identified for futuredevelopment as stated in the Third NationalAgricultural Policy 1998-2010 (Ministry ofAgriculture Malaysia 1999). The area ofcultivation is to be expanded and these cropswill be cultivated on a large commercial scalethroughout Malaysia. The aim of this study wasto determine the growth and physiologicalresponses of young mango and citrus plantsexposed to water deficit, as well as to improveunderstanding on the drought tolerancemechanism involved in the responses of thesefruit trees to water deficit The role of prolineand peroxidase in drought tolerance mechanismin both species was determined. The response ofplant on recovery to water stress was assessed bythe ability of plants to rejuvenate their vegetativestage.

MATERIAL AND METHODS

Eighteen months mango (Mangifera indica)cultivar Chukanan and fourteen months citrus(Citrus sinensis L) cultivar Limau Madu weregrown in plastic containers containing 40 kg ofsoil mixtures. The plants were grown in well-watered conditions for 6 weeks prior to water

stress treatments allowing roots to grow andbecome established in the bottom section of thecontainers. During this 42 -day period, plantswere watered daily until water drained freelyfrom the drainage holes at the bottom andfertilized weekly with full strength of CooperSolution (Cooper 1973). The experiment wasconducted at the Department of Crop Science,Universiti Putra Malaysia, Serdang, Selangor.

The experiment consisted of two soilmoisture treatments; control (well watered) andwater stress. In the well-watered control, plantswere irrigated daily until water drained freely. Inwater stress treatments, the whole soil in thecontainer was allowed to dry down by withholdingirrigation. Each group of watering treatmentsconsisted of twenty plants arranged in acompletely randomized design with fourreplicates. At each harvest, 4 plants were sampledfor destructive samplings of leaf water potentialand peroxidase determination. Soil moisturecontent was measured with a time domainreflectometry technique (Topp et al 1980). Afterthe drying cycle was completed, plants grownunder water stress condition were irrigated toobserve the potential of recovery on both plantsspecies.

Leal length increment was determined onthe leaves that were tagged before treatmentsbegan. The leaf length increments were calculatedat each sampling date by measuring the differencesbetween the length on the sampling date and theinitial measurements expressed in rate of leafincrement per day. The differential recovery ofmango and citrus were assessed by regenerationof new shoots from the plants.

The onset of responses of water deficit wasobserved by measuring leaf water potential atmid-day from one young fully expanded leaf perplant and four plant plants per treatment, usinga pressure chamber, following the recom-mendation of Turner (1986). Leaf stomatalconductance and net photosynthetic rate weremeasured at mid-day for a similar number andtype of leaves as for leaf water potential. Stomatalconductance was measured on the abaxial surfaceof leaf using a diffusive porometer (AP-4, Delta-T Devices Ltd, Cambridge, UK). The photo-synthesis rate was determined using a LCA-3portable infrared gas analyzer (LCA3, AnalyticalDevelopment Co. Hoddesdon, UK).

Peroxidase activity in the leaf tissue wasdetermined on the youngest fully-developed leaf

48 PERTANIKAJ. TROP. AGRIC. SCI. VOL. 27 NO. 1, 2004

DIFFERENTIAL RESPONSES IN M INDICA 8c C. SINENSIS L PLANTS TO WATER DEFICIT

sampled from both plant species. 0.5 g of leaftissue was homogonised with a mortar and pestle,using 1 ml cold 0.05M sodium acetate buffer(pH5.0). Five milligrams of polyvinylpyrrolidone(PVPP) was added to each sample in order todecrease interaction of phenol-proteins duringextraction. The homogenate was centrifuged at14000 Xg for 20 minutes at 4-6 C. The supernatantwas used to determine the enzyme activities.Extraction of ionically bound peroxidase wasperformed by re-homogenizing the pellets fromthe above extraction with the same buffercontaining 1M sodium chloride (NaCl). Sampleswere incubated at 4-5 °C for 24 h and centrifugedas described above. The peroxidase activities ofboth soluble and ionically bound supernatantwere determined. A 20 ml sample of thesupernatant was added to 3 ml of the assaymixture, which consisted of a solution of 0.1 Msodium phosphate buffer (pH6.0), lmMhydrogen peroxide (H202) and 0.1 mM )-methoxyphenol (guaiacol). The increase inabsorbance density at 470nm was recorded witha spectrophotometer (Spectronoc 20 Genessys)and the enzyme was expressed as the change inabsorbance per minute per gram fresh weight.Determination of free proline levels was basedon the method described by Bates et al (1973).Proline was extracted from liquid nitrogen -frozen tissue by homogenizing 5 g of the sampledleaves with 10 ml of 3% sulfosalicylic acid at 25C. The homogenate was filtered throughWhatman No 2 filter paper. Two ml of thefiltrate was reacted with two ml of glacial aceticacid and two-ml acid ninhydrin in a test tube forone hour in a water bath at 95 °C. The reactionmixture was then cooled in an ice bath. Followingthat, 4 ml of toluene was added to the reactionmixture and mixed rigorously with a test tubestirrer for 20 seconds. The toluene layer on thetop, which has a pink-red color, was collectedwith a pipette. The absorbency of the toluenelayer was read at 520 nm with a spectrophotometerusing toluene as a blank. Standard curve wasproduced ranging 0 to 30 ug/ml of L-proline(Sigma chemical Co. St Louis, Mo.) dissolved in3% sulfosalicylic acid. Proline standard curvewas used to calculate proline concentration insample on fresh weight basis.

RESULTSFig. 1 shows changes in soil moisture contentand rate of leaf length increment as influenced

by withholding water for 15 days. Soil moisturedeclined from 0.26 to 0.12 g cm'3 by withholdingwater for 15 days in the containers. This reductionin soil moisture content had significantly reducedthe rate of leaf length increment and plantphysiological processes. Under well-wateredconditions, leaf length increment was higher formango compared to citrus plants (Fig. 2). Thewell-watered mango plants grew steadily for thefirst six days of plants in the treatments.Thereafter, leaf expansion declined or plateaudas the leaf reached its maximum growth. Therate of leaf increment of water-stressed plantsdeclined progressively after day 3 of withholdingwater. The reduction in the rate of leaf lengthincrement in water-stressed mango plants hadresulted in a reduction of 8.84 cm in the finalleaf length compared to well watered plants. Incitrus, final leaf length was 2.1 cm shorter inwater-stressed compared in the well wateredplants. After rewatering, regeneration of shootswas faster in citrus than in mango plants (Fig. 3).

Fig. 4 shows changes in leaf water potential,stomatal conductance and photosynthetic rateof mango and citrus plants as influenced bywater stress. Leaf water potential shows asignificant difference between these two plantspecies. On the onset of water stress, leaf waterpotential of citrus declined rapidly compared tomango plants. Lower leaf water potential valuesin citrus were also observed for plants grown inwell-watered conditions. The change in stomatalconductance during water stressed periodfollowed quite a different pattern in comparisonto the leaf water potential. This reduction in leafwater potential had caused similar reduction instomatal conductance and leaf photosynthesisrate of plants exposed to water stress. Thereduction in stomatal conductance was greaterin mango than citrus plants. By day 6, stomatalconductance was reduced by 84% and 54 % inwater stressed mango and citrus, respectively.Further exposure to water stress, both mangoand citrus reached the same stomatal conductancevalues. The photosynthetic rate declinedprogressively with increased duration of waterstress in both mango and citrus plants. Therewere significant reductions in the photosyntheticrates in both water-stressed mango and citrusplants when measurements were made on day 3after withholding water. The results showedsimilar trends as observed in stomatal conductancewhere photosynthetic rate started to reach its

PERTANIKAJ. TROP. AGRIC. SCI. VOL. 27 NO. 1, 2004 49


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DIFFERENTIAL RESPONSES !NfvM. INDICA & C. SINENSfS L PLANTS TO WATER DEFICIT

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minimum values after 6 days of withholdingwater. Thereafter, the photosynthetic rateremained lower and reached the lowest valuesafter prolonged exposure to water stress in bothmango and citrus plants.

Measurements on peroxidase activity showsignificant higher values observed in water-stressed citrus compared to mango plants (Fig.5). In both species, proline content increasedwith exposure to water stress. There were markeddifferences in proline content between citrusand mango in both well-watered and water-stressed conditions. Higher concentration ofproline was observed in citrus compared to mangoplants. There was a 6-10 fold increase in prolinecontent when both species were subjected towater stressed conditions.

DISCUSSION

Leaf growth was very sensitive to the reductionin soil water availability. Rapid reduction in leafincrement suggests that available water is one ofthe major factors that determines growth ofmango plants at establishment in the field.Nonami and Boyer (1989) suggest that leafgrowth could be inhibited at low water potentialdespite complete maintenance of turgor in thegrowing region. However, the explanation forthis situation of growth inhibition might be

metabolically regulated through osmoticadjustment or cell wall associated enzymespossibly serving an adequate role by restrictingthe development of transpiring surface areas.Nevertheless, leaf growth of these plants speciesis sensitive to soil drying. In retrospect, leafgrowth can be influenced through the mechanismof non-hydraulic factor synthesis from the roots(Bacon et al. 1998) or inhibition of leaf growthas a result of decrease in cell wall extensibility(Lu and Newman 1998). The threshold value ofaround -1.20MPa and -0.95MPa can be observedbelow which leaf increment was almost zero incitrus and mango, respectively.

In this study, leaf water potential was usedas an indicator for water stress in both plantspecies. The decline in water availability bywithholding water had significantly reduced leafwater potential and stomatal conductance onboth plant species. In the water-stressed plants,minimum leaf water potential at midday wasaround -2.5 MPa and -2.0 MPa for citrus plants,respectively. The values of leaf water potentialmeasured here for stressed plants werecomparable with those usually reported for othercitrus species under severe stress in differentclimates (Kaufman and Levy 1976; Levy 1983).As shown in Fig. 4, stomatal conductance washigher in mango than citrus plants in well-

PERTANIKAJ. TROP. AGRIC. SCL VOL. 27 NO. 1, 2004 51


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Fig. 4: Changes in leaf water potential (Lwp). stomatak conductance )gs) and photosynthesis rate (pn)of mango (o) and citrus ( Q ) which were either well watered (closed symbol) and water

stress (open symbol). Bars represent ± SE of 4-5 replicates

watered plants. Both plant species showed nosignificant differences in stomatal conductancebetween stressed and control plants at 1 d afterwithholding water. Imposition of water stresshad resulted in a further reduction in stomatalconductance. The differences between both plantspecies were obvious on days 6 and 9 of imposingstress with a higher stomatal conductancerecorded on citrus compared to mango plants.

This could explain findings from the presentstudy that show a greater drought tolerance andrecovery at a faster rate after rewatering in citruscompared to mango plants. The results agreedwith the findings on drought tolerance ofEucalyptus clones that show that plants that havestrong stomatal control of water loss enablesrapid responses to changing conditions of wateravailability and possessed characteristics of


DIFFERENTIAL RESPONSES IN M. INDICA 8c C. SJNENSIS L PLANTS TO WATER DEFICIT

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Fig. 5: Peroxidase activity in mango (o) and ( • ) citrus which were either well watered (closed symbol)and water stressed (open symbol). Bars represent ± SE of four replicates

tolerance to environmental stresses (Farrell et al1996). The more drought tolerant species controlstomatal function to allow some carbon fixationat stress, thus improving water use efficiency oropen stomata rapidly when water deficit isrelieved (Yordanov et al 2000). There was asimilar trend of reduction in photosynthetic rateas in stomatal conductance with exposure ofplants to water deficits. The results clearlyindicate that stomatal limitation had contributedto a decrease in the photosynthesis rate. This isin agreement with Farquhar et al (1989) whoindicated that stomatal factors are moreimportant than non-stomatal factors in affectingphotosynthesis rate under water deficit, mainlybecause of leaf stomatal heterogeneity.

Water deficit can result in an increasedproduction of reactive oxygen species andtherefore requires elevated levels of antioxidantsfor stress compensation. The ability of plants toovercome the effects of different stresses and tosustain their productivity may be related toincreased enzymes such as super oxide dismutase,peroxidases and reductases (Polle andRennenberg 1994; Awad et al 2000). Theresponse of increase peroxidase activity with waterstress was clearly evident in citrus plants. Incontrast, the present study shows that waterdeficit did not cause a significant increase in

peroxidase activity in mango plants. Our resultson the insignificant effects of water stress tocaused elevation of peroxidase activities agreedwith other findings (Zhang and Kirkham 1996;Brown et al 1995; Fu and Huang 2001). Bothcitrus and mango plants were found toaccumulate proline when exposed to increasingwater stress (Fig. 6). Proline is considered to beinvolved in the adaptation mechanism in droughtstress. The accumulation of proline in plantsunder identical stress condition is species-specific(Heuer 1999). In Citrus macrophylla seedlings,proline accumu-lation was proportional to theseverity of water stress and not to leaf waterpotential (Levy 1983). As proline plays anosmoregulatory role in plants, species that canaccumulate higher proline levels during waterstress can be considered more tolerant to waterstress. Our data suggest that citrus accumulatedhigher proline and tended to survive water stressmore readily and regenerate shoots rapidlyfollowing stress relief compared to mango plants.

The present study shows the differentialplant responses to water deficit for both mangoand citrus plants. This is important in optimizingwater resources for cultivation of these plants inthe field conditions. A proper water managementneeds to be adopted in establishing mango plantsto avoid plant desiccation and mortality. The



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days after treatmentsFig. 6: Proline in mango (mango (o) and citrus ( Q ) which was either well watered (closed symbol)

and water-stressed (open symbol). Bars represent ± SE of 4 replicates

capability for adaptation to localized droughtstress can be related to a sustained stomatalconductance, higher proline and peroxidaseactivity in citrus than mango plants. Furtherstudies need to be conducted to identify thepossible candidate that controls leaf expansionand stomatal conductance for improvement ofwater use efficiency in mango and citrus plantsduring water deficit condition.

ACKNOWLEDGEMENTSThe authors thank the Ministry of Science,Environment and Technology, Malaysia forproviding the IRPA Grant 01-02-04-0509 forconducting this research. We thank UniversitiPutra Malaysia for their support and facilities.

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(Received: 25 September 2002)(Accepted: 7 January 2004)


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