Improved water use efficiency in rice under limited water environment ...

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Journal of Food, Agriculture & Environment Vol.12 (3&4): 149-154. 2014

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Improved water use efficiency in rice under limited water environment through microbial inoculation Mohamad Husni Omar 1*, Zulkarami Berahim 1, Norazrin Ariffin 1, Mohd Razi Ismail 1, 2, Halimi Mohd Saud 1, 3 , Nurul Amalina 1, S. H. Habib 2 and H. Kausar 1 Laboratory of Food Crops, Institute of Tropical Agriculture, 2 Department of Crop Science, Faculty of Agriculture, Department of Agriculture Technology, Faculty of Agriculture, Universiti Putra Malaysia, Serdang, Selangor, Malaysia. *e-mail: [email protected] 1

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Received 14 February 2014, accepted 10 September 2014.

Abstract An experiment was conducted to evaluate the potential of plant growth promoting rhizobacteria (PGPR) for enhancing yield and yield contributing characters of MR219 rice variety in limited water environment. A total of 20 bacteria were isolated from different dry rhizosphere soil samples. Nine isolates (A1, A4, A5, B4, C2, C3, D1, D2a and D3) were found to fix nitrogen by changing the colour of malate media into pale blue. Six isolates (A4, B2b, B4, C2, D2a and D4) developed halo zones on phosphate growth medium showing their ability to solubilize phosphate on such media. The significantly highest IAA was produced by the isolate D2a. Based on the results of in vitro screening test, two best performed isolates were further evaluated on rice variety MR219 under drought condition. The results of the glass house study revealed that, both the selected isolates B4 and D2a were effective in enhancing plant physiological and yield contributing characteristics over control treatment indicating their potential to be used as PGPR in rice variety MR219 under drought condition. Key words: Oryza sativa, PGPR, water stress, nitrogen fixation, phosphate solubilization, IAA.

Introduction Rice (Oryza sativa L.) is one of the staple foods for more than half of the world’s population. It accounts about 23% of the world’s caloric intake. The demand for rice production is increasing with the ever increasing world population 1, 2. About two-thirds of the total rice production comes from irrigated paddy land 3. Therefore, the present and future food security depends largely on irrigated rice production system. Rice is a profligate water user and semi aquatic in nature. Roughly it takes about 3,000 - 5,000 litres of water to produce 1 kg of rice, which is 2 to 3 times more than to produce 1 kg of any other cereal crops like wheat or maize 4. The conventional system of rice cultivation is flooded condition, which provides water and nutrient supply in anaerobic conditions and uses large amounts of water. However, about half of the rice growing area in the world does not have enough water to maintain flooded conditions, and yield is therefore reduced, to some extent, by drought. Drought at critical stage may result in considerable yield reduction and crop failure 2. In rain fed ecosystems, drought is a major limitation for rice production where timing and duration of drought is related to phenological process and rice yields 5. A challenge for sustainable rice cultivation is to decrease the usage of water while increasing or maintaining the yield. However, rice plants have relatively little adaptations to limited water and are extremely sensitive to drought 6, 7. In near future, many countries will face water problems for shortage, poor quality or flood that will increase regional tension. By 2030, without more efficient management of water resources, the present problem will hinder food production in many countries 8. Many breeding and genetic engineering strategies have been proposed to develop drought resistant variety but the approaches

are slower than expectation due to genetic complexity to stress responses. Therefore, different alternatives rather than irrigation strategy should be explored to achieve the aim. Microorganisms existing in plant rhizosphere offer new opportunity for agricultural biotechnology 9. Plant growth promoting rhizobacteria (PGPR) influence plant health and productivity by solubilization of mineral nutrients, stimulation of root growth and suppression of root diseases 10. Recently, few reports have been published on PGPR as elicitors of tolerance to abiotic stresses such as drought, salt and nutrient deficiency or excess 11-13. Beneficial microbes or PGPR are free-living soil bacteria that can either directly or indirectly facilitate or confer beneficial effects to plants, such as increased plant growth and reduced susceptibility to diseases caused by plant pathogenic fungi, bacteria, viruses and nematodes. These PGPR include Azospirillum, Pseudomonas, Bacillus, and Agrobacterium species. PGPR also can protect plants from the deleterious effects of some environmental stresses including heavy metals, flooding, salt, and phytopathogens. Relatively, few mechanisms have been clearly demonstrated to explain the increased resistance to environmental stresses including water stress of plants treated with PGPR 14. Previous research by using PGPR that confer resistance to water stress in tomatoes and peppers showed that the PGPR can facilitate plant growth in stress environment 15. Herman et al. 16 also reported enhanced physiological responses of sweet pepper with inoculation of PGPR and mycorrhiza. However, there are lack of information in rice growth and production by using beneficial PGPR under water stress environment. So, the aim of this study was to evaluate the effectiveness of PGPR to improve water use

Journal of Food, Agriculture & Environment, Vol.12 (3&4), July-October 2014

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efficiency of rice under limited water environments. Materials and Methods Isolation and screening of bacterial strains: Plant growth promoting rhizobacteria (PGPR) were isolated from dry rhizosphere soil samples collected from Tanjung Karang paddy field, Selangor, Malaysia. Soil samples consisted of five cores randomly taken from five cm depth and pooled into clean plastic bags. Samples were stored at 4°C until use. Ten grams of soil sample was added with 90 ml of sterile saline water (0.85% NaCl) and agitated at 150 rpm for 30 min. Serial dilutions from 10-2 to 10-7 were prepared by sequentially transferring 1 ml diluted sample into each test tube containing 9 ml of sterile saline water. A 100 µl of sample at selected dilutions was transferred onto Yeast Extract Mannitol (YEM) agar plate [1.0 g yeast extract, 10.0 g mannitol, 0.5 g K2HPO4, 0.2 g MgSO4.7H2O, 0.1g NaCl, 20.0 g agar and 1.0 L distilled water; pH 6.5] and incubated at 28 - 30°C for 24 h. The samples were spread over media using a sterilized bent glass rod. The plates were examined regularly. Bacterial single colonies were prepared by touching and streaking on Yeast Extract Mannitol (YEM) agar plates in a third streak pattern. Isolated single colony was picked up and re-streaked onto fresh YEM agar plates and incubated similarly. Pure cultures were kept as stock at 4°C until required for further studies. In vitro screening for plant growth promoting activities: Isolated bacterial strains were tested for plant growth promoting activities such as nitrogen fixation, phosphate solubilization and indole-3acetic acid (IAA). Determination of nitrogen-fixing ability: Nitrogen fixing ability was tested using the media proposed by Jha et al. 17. All isolated bacteria were cultured in N-free semisolid malate medium containing per litre 5 g malic acid, 0.5 g K2HPO4, 0.2 g MgSO4.7H2O, 0.1 g NaCl, 0.02 g CaCl2.2H2O, 4.0 g KOH, 1.8 g agar with addition of 2 ml micronutrient, 4 ml FeEDTA, 1 ml vitamin solution, pH 6.5]. The agar will turn into pale blue with growth of nitrogen-fixing bacteria. Determination of phosphate solubilization activity: Phosphate (P) solubilization test was conducted using NBRIP media [10 g glucose, 5 g Ca3(PO4)2, 5 g MgCl2.6H2O, 0.25 g MgSO4.7H2O, 0.2 g KCl, 0.1 g (NH4)2SO4, 15 g agar and 1.0 L distilled water, pH 6.5] containing tri-calcium phosphate. This medium was chosen as it was reported to be more efficient in screening phosphate solubilizing microorganisms than Pikovskaya medium 18. Bacterial isolates were cultured in NB for two days and 10 µl was spotted on the surface of media plates by using a micro pipette. The plates were incubated at 30°C for one week. Halo zones around the bacterial colonies indicate phosphate solubilization. The size of the halo zones was determined by measuring the radius formed around colonies. Determination of indole-3-acetic acid (IAA): All bacteria isolates were grown in Nutrient Broth (NB) on an incubator shaker (150 rpm) at room temperature (28 ± 2°C) for 24 h. After the 24 h incubation, 1 ml of bacterial culture was inoculated into 100 ml of sterile NB amended with 5 ml L-tryptophan solution and allowed to grow for 48 h. Flasks containing un-inoculated media were 150

used as controls or blanks. To determine the amount of IAA produced from the isolates, 1.5 ml of aliquot was sampled and centrifuged at 12,000 rpm for 5 min. One ml of the supernatant was added to 2 ml of Salkowski reagent (ferric chloride and perchloric acid). After 25 min of incubation the colour density of the mixtures was read using UV-spectrophotometer (Model UV-3600, Shimadzu) at 530 nm absorbance. The amount of IAA produced was determined using the standard curve. Plant material and experimental design: The experiment was conducted at glass house, Universiti Putra Malaysia, from April 2011 to August 2011. Rice seeds of variety MR219 obtained from GeneBank, MARDI Research Station, Pinang, Malaysia, were used in this experiment. Seeds were surface sterilized, soaked in water and Zappa Plus for 24 h, subsequently sown in silty clay soil for germination. The soil used in this study was collected from Tanjung Karang, Selangor, Malaysia, belongs to Bernam soil series. The soil was rich in P, K, Ca, Mg and Zn and with a pH of around 5.01 which is suitable for rice cultivation. The soil was spread on the green house floor, air dried, crushed and sieved through a 5.0 mm mesh to remove gravels and large debris. A 2.5 kg of air-dried soil was packed into plastic bags and sterilized by gamma ray (40 kGy). Then the soil with plastic bag was placed in the plastic pot (25 cm × 17 cm) and the soil was soaked with distilled water for 2 days. Each pot was fertilized with 120-70-80 kg ha-1 N-P-K, and the sources were urea, triple super phosphate, and muriate of potash, respectively, in four instalments at 15, 35, 55 and 70 DAT. After 15 days of germination rice seedlings were transplanted into pots according to the treatments (Table 1). After transplanting, plants were maintained under well-watered condition until 15 days and the drought treatments (watering interval) were started. Table 1. Treatments used in this experiment. Treatments T1 T2 T3 T4 T5 T6 T7

Flooded condition Watering at 5 days interval Watering at 5 days interval + Isolate B4 Watering at 5 days interval + Isolate D2a Watering at 10 days interval Watering at 10 days interval + Isolate B4 Watering at 10 days interval + Isolate D2a

The experiment was laid out in a randomised complete block design (RCBD) with three replications. Selected PGPR was grown in YEMA medium on rotary shaker. At log phase of growth, bacterial suspension was centrifuged at 10,000 rpm for 4 min and washed three times in phosphate buffer. Bacterial concentration was adjusted at 108 cfu ml-1 19, 20. Two ml of each bacterial isolate (B4 and D2a) was applied to respective plant at the transplanting time and 10 days later. Harvesting, data recorded of the plants and analysis: Data on chlorophyll content and photosynthesis rate were also recorded by using SPAD meter and Li-Cor LI-6400XT portable photosynthesis system, respectively. At the end of the experiment, plants were harvested and rice yield components, such as total panicles, length of panicles, total spikelets, and total filled spikelets, were recorded.


Statistical analysis: The data was subjected to analysis of variance (ANOVA) and tested for significance using least significant difference (LSD) by PC-SAS software 9.0 at 5% probability. Results Isolation, screening and plant growth promoting (PGP) activities: A total of 20 bacteria were isolated from different rhizosphere soil samples. All isolates were analysed based on their cultural and morphological characteristics, i.e., colony morphology, colour, shape and growth patterns. All bacterial isolates exhibited different efficiency to nitrogen fixation, phosphate solubilization and IAA production when tested on N-free semisolid malate medium, phosphate growth medium and NBRIP phosphate growth medium with L-tryptophan (Table 2, Figs. 1-3).

Table 2. Ability of PGPR isolates of nitrogen fixation, solubilization of phosphate, and production of IAA on N-free semisolid malate medium, phosphate growth medium and NBRIP phosphate growth medium with L-tryptophan. Isolates A1 A2(a) A2(b) A3 A4 A5 B1(a) B1(b) B2(a) B2(b) B3 B4 C1 C2 C3 D1 D2(a) D2(b) D3 D4

Plant growth promoting characteristic Nitrogen Phosphate IAA fixation solubilization production ++ + +++ + + ++ + + +++ ++ ++ + + +++ ++ + ++ +++ ++ ++ +++ + +++ + + +++ + +++ + +++ ++

- = No production; + = weak producer; ++ = medium producer; and +++ = good producer.

Nine isolates were found to turn N-free semisolid malate medium into pale blue. Among them, four isolates (A5, B4, C2 and D3) showed higher ability to fix nitrogen by changing the color of malate media into pale blue. Three isolates (A1, A4 and C3) showed intermediate potential whereas two isolates (D1 and D2a) showed the lowest potential to fix nitrogen in in-vitro screening test (Table 2, Fig. 1). Six isolates (A4, B2b, B4, C2, D2a and D4) developed halo zones on phosphate growth medium showing their potency to solubilize phosphate on such media. Among them, isolate D4 appeared as best and produced the biggest halo zone on NBRIP growth medium. Isolate B4 and C2 were categorized as intermediate while B2b and D2a produced the smallest halo zone on NBRIP growth Figure 2. Ability of PGPR isolates to solubilize phosphate on phosphate growth medium. medium (Table 2, Fig. 2). Out of 20 bacterial isolates, 15 were found to 25 produce IAA. The significantly highest IAA was produced by the isolate D2a (20.7 µg/ml) 20 which was closely followed by the isolate A2a (20.4 µg/ml). The least amount of IAA was produced by the isolate D2d, followed by B2a, 15 A1 and A3. On the other hand, four isolates (A5, B2b, B3 and B4) did not produce IAA on 10 L-tryptophan added NBRIP phosphate growth medium (Table 2, Fig. 3). Different treatments exhibited significant 5 differences in chlorophyll content and photosynthesis (Table 3). The results showed 0 that plants treated with T4 and T1, showed the A 1 2(a) 2(b) A 3 A 4 A 5 B1(a) 1(b) B2(a) 2(b) B3 B4 C1 C2 C3 D 1 2(a) 2(b) D 3 D 4 B A A B D D significantly highest chlorophyll content and Isolate photosynthesis compared to other treatments. In all plants, chlorophyll content ranged from Figure 3. Ability of PGPR isolates to produce IAA on NBRIP phosphate growth medium 34 to 44. Treatments T1 and T4 showed the with L-tryptophan.

IAA concentration (µg/ml)

Figure 1. Ability of PGPR isolates to fix nitrogen on N-free semisolid malate medium.


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Table 3. Effect of different treatments on chlorophyll content and photosynthesis of rice. Treatment T1 T2 T3 T4 T5 T6 T7

Chlorophyll content (Time, unit) 44 a 37 b 43 a 44 a 34 b 35 b 36 b

Photosynthesis (Time, unit) 15 a 13 b 14 b 16 a 12 b 13 b 13 b

Values having the same letter(s) in a column do not differ significantly at the 5% level of probability.

significantly highest chlorophyll content followed by T3and T7. On the other hand, the significantly lowest chlorophyll content was recorded in plants treated with T4 which was closely followed by T6. Similar to chlorophyll content, the significantly highest photosynthesis was recorded in plants treated with T4 followed by T1. However, the least photosynthesis was recorded in plants treated with T5 treatment. Results show that panicle number, panicle length, spikelet number and percentage of filled spikelets were higher in plants treated with T4 (Table 4). The highest panicle number was recorded in treatment T4, followed by T1, T3 and T6, respectively, whereas it was lowest in treatments T5 and T7, respectively. The highest panicle length was found in treatment T4, closely followed by T1, T3 and T6, respectively, whereas it was least in treatment T5. The significantly highest spikelets number was recorded in plants receiving treatment T4, followed by T5, T6 and T7, respectively. The significantly least spikelets number was found in plants receiving treatment T1. The highest number of filled spikelets was found in treatment T4 closely followed by T1 and T3, whereas it was least in treatment T6. Table 4. Effect of different treatments on growth and yield contributing characters of rice. Treatment T1 T2 T3 T4 T5 T6 T7

Number of panicles 16 a 15 ab 16 a 17 a 14 b 15 ab 14 b

Panicle length (cm) 26 a 25 a 26 a 27 a 24 a 25 a 26 a

Number of spikelets 174 c 185 bc 196 bc 229 a 209 b 209 b 204 b

Filled spikelets (%) 70.3 a 60 .0 b 70.1 a 70.9 a 50.8 bc 50.0 c 52.8 c

Values having the same letter(s) in a column do not differ significantly at the 5% level of probability.

Discussion Plant growth-promoting microorganisms (PGPM) are known to influence plant growth by various direct mechanisms through production of plant hormones, improved mineralisation, increased iron uptake and promoted plant growth and indirect mechanisms through the production of siderophores, antibiosis, lysis of pathogen cell walls and elicit induced systemic resistance (ISR) in various crops including cereals 21. The tropical soils of Malaysia harbour diverse groups of plant growth promoting bacteria. In this study, out of 20 isolates, nine were found to turn N-free semisolid malate medium into pale blue 152

indicating they have the ability to fix atmospheric nitrogen in such medium. Large amounts of nitrogen derived from biological fixation have been shown to be present in rice plants 22. They utilize rhizosphere carbon compounds for growth and development and subsequently fix nitrogen for the plant. Besides consequences of nitrogen fixation, bacteria exhibit plant growth enhancement activities such as production of phytohormones, antifungal or antibacterial agents, siderophore and induction of systemic acquired host resistance and increased availability of mineral nutrients to plants 23. Azorhizobium caulinodans enters into the root system of cereals by intercellular invasion between epidermal cells and the xylem. The xylem colonization might provide a nonnodular niche for endosymbiotic nitrogen fixation in rice, wheat, maize, sorghum and other non-legume crops 24. Vascular tissue is an ideal niche for endophytic colonization as there is low partial pressure of oxygen (pO2) and allocation of photosynthate. Application of Rhizobium leguminosarum bv. trifolii has been shown to successfully colonize rice roots and supplied 25 - 33% of the recommended rate of N fertilizer 25. In vitro screening results revealed that the production of IAA varied with all the isolates tested. Isolate D2a produced the significantly highest amount of IAA. IAA is one of the phytohormones, considered as the most physiologically active auxin in plants that influences root and shoot dry matter partitioning, root and shoot elongation through cell wall extension 26. These results were in agreement with Mirza et al. 27 who reported variations among different species and strains, as well as the effects of culture conditions, growth stage and substrate availability. The capability of PGPM in producing IAA appears to be important mechanisms involved in promoting plant growth. The application of Trichoderma spp., Enterobacter spp. and Bacillus spp. as PGPM to enhance plant growth has been reported to be related to the synthesis of plant growth hormones like IAA 28. These findings are also supported with those by Zarea et al. 29 who demonstrated that seeds inoculated with IAAproducing microorganisms significantly enhanced early seedling establishment. IAA is an important phytohormone produced by PGPM that increased shoot growth, root hair density and length 30, enhanced rice seed germination and improved growth 31. Plant water and nutrient uptake potential is closely related to root growth such as root surface area especially under dry cultivation systems. Mantellin and Touraine 32 and Mia et al. 33 who demonstrated that phytohormone produced by microbes caused morphological and physiological changes in root, and resulted in increased nutrients and water uptake from the soil. The greater growth stimulation and vigour of young seedlings with pre-inoculation would result in better productivity and higher yields at maturity 34. Application of phosphate-solubilizing microorganisms (PSM) is essential for increasing P uptake for plant growth. In this study, 15 out of 20 bacterial isolates showed positive P-solubilization. Among them D4 appeared as the most promising PSM on NBRIP growth medium. Most Pseudomonas and Bacillus isolates are involved in solubilization of inorganic phosphorus 35. However, according to Eusuf Zai et al. 36, although P-solubilizing bacteria outnumber P-solubilizing fungi in soil, fungi isolates generally exhibit greater P-solubilizing ability than bacteria in both liquid and solid media. Phosphorus (P) is an essential plant nutrient for plant growth. However, only a small part of P is utilized by plants, while the rest is converted into insoluble fixed forms 37. P deficiency


is usually the consequence of low intrinsic P fertility due to weathering, in combination with intensive, and nutrient-extracting agricultural practices. Moreover, phosphate diffusion to plant roots may be too low to meet the requirements of the crop if soils have low P solubility and a high P fixation capacity 38. Almost 75 to 90% of added P fertilizer in agricultural soils is precipitated by iron, aluminium and calcium complexes present in soils 39. Furthermore, phosphatic fertilizers are expensive, and excessive use of rock phosphate (RP) is potentially and environmentally undesirable. Among microbial populations in soils, phosphate solubilizing bacteria (PSB) constitute solubilization potential of 1 to 50% 40. The mechanism involves solubilization of the phosphate in the presence of organic acids released by microorganisms 41. The most powerful P solubilizers were reported to be bacterial strains from the genera Pseudomonas, Bacillus, Rhizobium and Enterobacter along with Penicillium and Aspergillus fungi 42. Rice plant inoculated with isolates B4 and D2a demonstrated higher effects in plant growth promoting characteristics, such as chlorophyll content and photosynthesis rate, resulting in yield increments of rice variety MR219. In in-vitro screening test both of the isolates were found to fix nitrogen, solubilize phosphate and produce phytohormone IAA on N-free semisolid malate medium, phosphate growth medium and NBRIP phosphate growth medium with L-tryptophan. The results obtained in this study confirmed that rice plants treated with either T4 or T3 accumulated higher dry matter which contributed higher yields. These results (obtained from treatment T4) were comparable with normal flooding condition (treatment T1). However, an integration of several microorganisms may provide a more significant reliable effect in both protections against pathogens and also as plant growth promoter 43. The use of organic amendments is also recommended to support the growth of the inoculums. In the current study, therefore, isolates B4 and D2a could be selected as microbial consortium to promote plant growth and drought tolerance. Conclusions The results indicate that the plant growth promoting rhizobacteria isolated from different rhizosphere soil samples were able to enhance growth promoting, physiological and yield contributing characteristics of rice variety MR219. Out of 20 different isolates, two isolates, B4 and D2a, showed optimum plant growth promoting activities on N-free semisolid malate medium, phosphate growth medium and NBRIP phosphate growth medium with Ltryptophan. Glass house trial also showed that both of the selected isolates enhanced plant growth, yield and yield contributing characters in drought condition compared to control. Acknowledgements The authors would like to acknowledge the support of Universiti Putra Malaysia (UPM) Research University Grant and the Ministry of Education, Malaysia Long Term Research Grant Scheme (LRGS) - Food Security-Enhances sustainable rice production for financial support without which this research would have been impossible. References Jeon, J. S., Jung, K. H., Kim, H. B., Suh, J. P. and Khush, G. S. 2011. Genetic and molecular insights into the enhancement of rice yield potential. J. Plant Biol. 54:1-9. 2 Bernier, J., Atlin, G. N., Serraj, R., Kumar, A. and Spaner, D. 2008. 1

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