Abstract
Bacterial isolates Achromobacter, Ochrobactrum Pseudomonas, and Variovorax have often been isolated from plant roots, and most of them have been described as growth enhancing rhizobacteria. These rhizobacteria have been used to boost crops productivity in varied region of agro-climatic regions. To lessen the usage of chemical fertilizers inputs and improve the sustainability of rice–wheat crops, this study was planned to investigate the impacts of bacterial consortium inoculants producing 1-aminocyclopropane-1-carboxylate (ACC) deaminase on plant growth, nutrient content and grain yield in a field trial. Rice and wheat plants subjected to plant growth-promoting rhizobacteria (PGPR) consortia of strain DPC9 (Ochrobactrum anthropi) + DPB13 (Pseudomonas palleroniana) + DPB15 (Pseudomonas fluorescens) + DPB16 (Pseudomonas palleroniana) gave the best results with reference to macronutrient—nitrogen, phosphorus, potassium, calcium and sodium content and yield-related parameters including 1000 grain weight (10.2%, 40.7%), number of grains per panicle/spike (45.5%, 60.6%), and tillers (32.2%, 106.6%). This inoculants significantly increased grain yield (65.6%, 74.4%), straw yield (26.8%, 36.9%) and harvest index (14.9%, 13.8%) of rice–wheat crops, respectively, when compared to their counterpart control plants. Significant positive correlation in parameters which contribute in producing high grain yield in rice–wheat include plant height (r = 0.938, r = 0.852), tillers (r = 0.968, r = 0.881), panicle/spike length (r = 0.844, r = 0.912), number of grains per panicle/spike (r = 0.969, r = 0.815), 1000 grain weight (r = 0.833, r = 0.931), straw yield (r = 0.920, r = 0.918) and harvest index (r = 0.909, r = 0.847) and also surge nutrient enhancement in rice and wheat were observed in consortium treated plants. It can be concluded that consortium of DPC9 + DPB13 + DPB15 + DPB16-producing ACC deaminase can serve as a useful bio-inoculant for sustainable rice–wheat production in diverse agro-ecosystem.
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Introduction
An approximately 13.5 million hectare area of Indo-Gangetic Plains is utilized for RWCS (rice–wheat cropping system) in south Asian countries. The proportion of this area is 10.0 million ha in India and rest 3.5 (2.2, 0.8, 0.5) shared in Pakistan, Bangladesh and Nepal, respectively. RWCS covers about 33% of the total rice area and 42% of the total wheat area and this is dominant cropping system in most of the Indian states (Mahajan and Gupta 2009; Kumar et al. 2014a, b; Sharma et al. 2015). Rice (Oryza sativa L.) and wheat (Triticum aestivum L.) are the staple food crops for more than 50% and 35% of the world’s population, respectively. Global production of wheat and rice is 772 millions of tonnes (FAOSTAT 2017) and 688.2 millions of tonnes (FAOSTAT 2018), respectively. Rice and wheat have contributed enormously to global food security and sustain humanity largely by enhancing the yields and by making them more robust in the face of abiotic and biotic stresses. Increased applications of chemical fertilization and pesticides have a negative effect on soil quality and soil microbial community. Moreover, excessive chemical fertilizer exaggerates the deterioration of soil organic matter and fertility and hastens soil acidification, which in turn reduces crop productivity (Li et al. 2017). The application of bio-inoculants in agricultural system is of strategic concern for their potential to lessen the usage of synthetic chemical fertilizers and pesticides and improve environment sustainability (Cortivo et al. 2020; Kantachote et al. 2016). Plant beneficial microbes referred to as PGPR that interact with roots of plants and augmented plant growth by enhancing nutrition acquisition and imparting resistance and tolerance to various stresses (Nadeem et al. 2013; Gupta et al. 2015).
PGPR’s are an essential part of rhizospheric biota that colonizes root of plants and escalate the growth and productivity of crops (Jorquera et al. 2012; Qessaoui et al. 2019; Chandra et al. 2019b). They improve plant growth through direct and indirect mechanisms (Adesemoye et al. 2009; Chandra et al. 2015, 2018a,b). Numerous studies revealed that substantial evidence for the beneficial effects of PGPR on plant growth under controlled conditions (Chandra et al. 2019a, 2020), and not efficient in the field conditions possibly due to unable to adequate colonization with plant roots and/or to compete with the inhabitant root microbiome (Kamilova et al. 2005; Dal Cortivo et al. 2017). The growth-promoting microorganisms need to be introduced in appropriate quantities that efficiently colonize roots of plant, as this is decisive step for their success in agroecosystems (Bishnoi 2015; Dal Cortivo et al. 2020). Subsequent biofertilizers application, it can be expected no interaction, positive and negative interaction with the resident bacterial population (Brimecombe et al. 2007).
Microbial inoculants represent a viable tool for improving growth and productivity of crops including rice and wheat. Different researchers reported the beneficial impact of rhizobacteria on rice are Bacillus spp. (Guyasa et al. 2018; Rais et al. 2018), Pseudomonas fluorescens (Guyasa et al. 2018), Serratia spp. (Nascente et al. 2019), Serratia nematodiphila (Chakraborty et al. 2013) and on wheat are Azotobacter chroococcum N9 (Wang et al. 2020), Achromobacter insolitus IAC-HT-11 (da Silveira et al. 2016), Pseudomonas sp. UW4, Pseudomonas palleroniana DPB16 and Variovorax paradoxus RAA3 (Chandra et al. 2019b). Therefore, this study evaluated the impact of bacterial consortia producing ACC deaminase together with other plant growth-promoting attributes on growth, nutrients and yield components of rice and wheat.
Materials and methods
Bacterial strain
Of the total ten bacterial strains were taken, out of eight described by Chandra et al. (2019a, b) and other two bacterial strain R81 (Pseudomonas synxantha) described by Mathimaran et al. (2012) and UW4 (Pseudomonas sp.) described by Duan et al. (2013) were used in different combination based on their compatibility. These strains exhibited multiple growth-promoting attributes such as ACC deaminase, indole 3-acetic acid (IAA) production, P-solubilization, ammonia production, N2 fixation and siderophore production are given in Supplementary Table SI.
Plant material and seed sterilization
In this experiment, two different varieties of rice (Swarna and Swarna Sub1) and wheat (WH 1105 and HD 2733) were taken to see the response of rice and wheat toward inoculation with PGPR consortia having ACC deaminase activity and other PGP (plant growth promoting) traits in field conditions. Seeds of rice and wheat were obtained from IRRI, New Delhi, India and DWR Karnal, Haryana, India, respectively. For the trial, the seeds were surface decontaminated by dipping the seeds in 0.1% of HgCl2 for 3 min followed by washing with 3–4 times and then 70% ethanol for 1 min followed by rinsing with sterile distilled water 5–6 times.
Soil physicochemical analysis
The field trial was conducted on vertisol clay soil of BSPC GBPUA&T Pantnagar and have physicochemical properties—pH (7.26), organic carbon (1.36%), nitrogen (261.61 kg/ha), phosphorus (18.57 kg/ha) and potassium (230.72 kg/ha). Before seeding, soil physiochemical properties (0–20 cm) from experimental fields were done using established methods. The soil pH was done according to the method of Beckman Glass electrode pH meter (Jackson 1973), organic carbon as per Walkley and Black (1934), total nitrogen by Kjeldahl digestion (Pelican Kelplus Kelvac VA equipment), available potassium by Flame photometery and available phosphorus by Olsen’s method (Olsen 1954).
Organic manure used
Before designing the experiment, Sesbenia aculeata (Dhaincha) as organic manure was sown in the field @ 20 kg/ha. The above-ground biomass of 45 days of standing crop of Sesbenia puddled properly into the pre-irrigated field 10 days before rice planting with the help of tractor. After harvesting of rice, for wheat trial, each plot of previously sown rice were dug out with the help of Grubbing hoe (phawda) to prevent the mixing of soil between plots. Same treatments were applied in each plot as in previously sown rice.
Raising nursery
Eighteen raised nursery beds for two varieties of rice having a dimension of 4 m2 providing 50 cm channels all around were prepared well before sowing of seed. The nursery beds were prepared with a massive mixture of soil. The seeds were sown @ 100 kg/ha in the raised bed, whereas the seeding rate for wheat was 90 @ kg/ha. The seeds were primed with PGPB containing ACC deaminase activity before sowing.
Experimental detail
The experiment was carried out during kharif and rabi season of 2015–2016 for the rice and wheat, respectively, at the BSPC, GBPUA&T, Pantnagar, U.S. Nagar, Uttarakhand, India. The experiment was accomplished in a randomized block design (RBD) with eight treatments and three replicates (Table 1).
Field preparation for transplanting
In the month of July, after proper mixing of standing crop of Sesbenia into soil field was properly levelled. Thereafter, the layout was made and bunds were constructed for separating the plots to prevent leaching of PGPB between the plots having different treatments. One day before transplanting, the field was flooded with water and puddled manually with the help of Grubbing hoe.
Bio-inoculants
On the basis of glass house study (Chandra et al. 2019a), seven bacterial consortium were further taken (Table 1) for the field trials to see the response of rice and wheat toward inoculation with PGPB containing ACC deaminase trait. The bacterial treatment for rice was given twice, at the time of seed sowing (seed treatment) and at the time of transplantation (seedling treatment) while for the wheat, bacterial treatment were given only once. The seeds (rice and wheat) were coated with charcoal-based PGPB cultures (107–108 cfu g−1 carrier) and left for 30 min for air drying then sowing in the prepared plot of each treatment. Another treatment was given to rice seedling at the time of transplantation. The rice seedlings were uprooted and roots of plants coated with charcoal-based PGPB cultures (107–108 cfu g−1 carrier).
Transplanting
After treatments, the seedlings were sown in their respective plots. Two seedlings were transplanted per hill and the distance between two hills was 25 cm. Light irrigation was given after 2 days of transplanting while for wheat, treated seeds were directly sown.
Water management and weed control
Soil was kept moist or slightly flooded during all the growth phase of rice. Water supply was stopped just before harvesting. The weeds were removed from field by hand at regular intervals.
Harvesting and threshing
At the maturity of rice–wheat crops, growth- and yield-related parameters were measured. A sampling area of 1 m2 in the centre of each experimental plot (area left after removing border plants) was harvested manually and day after the harvesting the plants from each plots were threshed by Pullman thresher and individual plot yields were noted.
Nutrient analysis of rice and wheat straw
For both the crops, straw sample were taken for nutrients (N, K, P, Ca and Na) analysis. Phosphorus content of straw was estimated as per the method described by Jackson (1973). The K, Ca and Na contents were estimated by Flame photometry and N content was determined by Kjeldahl digestion.
Statistical analysis
The collected data were subjected to two way ANOVA using SPSS (IBM SPSS statistics 20). Treatment comparisons of mean values were carried out using DMRT at a significance level of p < 0.05.
Results
Present study deals with ten bacterial strains that were used in different combination/consortium for their contribution to the growth promotion, nutrient content and yield components of both RWCS. In this experiment, two varieties of rice (Swarna and Swarna sub1) and wheat (WH 1105 and HD 2733) were taken.
Growth and yield components of rice and wheat
ANOVA results revealed that irrespective of treatments, Swarna variety showed significant differences for the plant height, total tillers, effective tillers, number of grains/panicle and grain yield. Among treatments, irrespective of varieties, treatment T8 (a consortium of DPC12 (Pseudomonas sp.) + PSA7 (A. marplatensis) + PSB8 (Achromobacter sp.) + RAA3 (V. paradoxus) and T7 (a consortium of DPC9 (Ochrobactrum anthropi), DPB13 (Pseudomonas palleroniana), DPB15 (Pseudomonas fluorescens), DPB16 (Pseudomonas palleroniana) producing ACC deaminase showed maximum increase 22.8% and 22.4%, respectively, in plant height when compared to non-treated control plants. We also noticed that treatment T7-treated plants exhibited 32.2% increase in numbers of tillers, 49.7% increase in effective tillers, 45.5% increase in numbers of grains/panicle, 21.0% increase in panicle length (Table 2), 10.2% increase in test weight/1000 grain weight, 65.6% increase in grain yield, 26.8% increase in straw yield and 14.9% increase in harvest index as compared to control plants (Fig. 1). When we compared all the treatments within varieties, treatment T8-treated plant indicated maximum enhancement in plant height and effective tillers and treatment T7-treated plants displayed grains/panicle, higher panicle length, grain yield, straw yield and 1000 grain weight, in Swarna, whereas T7-treated plants of Swarna sub1 showed the higher HI (data not shown).
Similarly, the ANOVA results revealed that irrespective of treatments, WH 1105 showed significant differences for 1000 grain weight, plant height, numbers of grains/spike, total tillers/plant, grain yield and straw yield than HD 2733. These wheat varieties showed non-significant differences for spike length and harvest index. All treated plants exhibited significant differences for plant height and spike length as compared to control. For most of the studied parameters, T7-treated plant exhibited significantly higher numbers of tillers (106.6%) and no. of grains/spike (60.6%) (Table 3) 1000 grain weight (40.7%), grain yield (74.4%), straw yield (36.9%) and harvest index (13.8%) as compared to non-inoculated control plants (Fig. 2). Among all the treatments within varieties, treatment T7 maximally increased plant height, total number of tillers, number of grains/spike, 1000 grain weight, grain yield, straw yield in WH 1105 and harvest index in HD 2733 (data not shown).
Correlation coefficient among yield and yield components in rice
We have noticed the positive correlation between the rice–wheat grain yield and yield-related components indicate that parameters which contribute in producing high grain yield include plant height (r = 0.938, r = 0.852), tillers (r = 0.968, r = 0.881), panicle/spike length (r = 0.844, r = 0.912), number of grains per panicle/spike (r = 0.969, r = 0.815), 1000 grain weight (r = 0.833, r = 0.931), straw yield (r = 0.920, r = 0.918) and harvest index (r = 0.909, r = 0.847) (Tables 4, 5).
Path coefficient analysis for rice and wheat
In this study, the response variable grain yield (GY) and seven predictor variables (plant height, tillers, panicle/spike length, no. of grains per panicle/spike, test weight (1000 grain weight), straw yield and harvest index) were taken for path coefficient analysis in rice and wheat. This analysis is performed to unveil the causes and effects of chain relationships of different yield contributing characters with grain yield. Assessments of direct and indirect effects of yield contributing characters on grain yield are presented in Tables 6 and 7.
Nutrient analysis of rice and wheat straw (N, P, K, Ca and Na)
Both rice varieties, irrespective of treatments, showed non-significant differences for sodium and phosphorus content, while Swarna variety showed significant differences for nitrogen and potassium, and Swarna sub1 for calcium content. However, the maximum NPK content in response of bacterial application was observed in the treatment T7 (2.75-, 2.12-, 2.09-fold) as compared to control. However, the maximum calcium and sodium content was found in the treatment T8 (1.45-fold) and T3 (1.62-fold), respectively, as compared to control plants (Table 8). When we compared all the treatments within varieties, T7-treated plants of Swarna showed maximum NPK content than Swarna sub 1, whereas T6- and T7-treated plants of Swarna sub1 showed maximum calcium and sodium content, respectively, than Swarna (data not shown).
In case of wheat, irrespective of treatments, variety WH 1105 showed significant differences for foliar nitrogen, potassium and calcium content and non-significant differences for phosphorus and sodium content. However, the maximum NPK content in response of bacterial application was observed in the treatment T7 (3.39-, 5.00-, 2.04-fold) as compared to control (Table 9). Within treatment bio-inoculant-treated plants exhibited little bit higher calcium and sodium content as compared to untreated control. When we compared all the treatments within varieties, T7-treated plants of WH 1105 showed higher nitrogen and potassium content, treatment T4- and T6 (both 0.59%)-treated plants of WH 1105 showed higher calcium content, whereas T7-treated plants of HD 2733 showed higher phosphorus content. Many of the treatments showed similar effect for sodium content when comparing treatments within varieties (data not shown).
Discussion
The consortium application of bacterial strains put forth a significant impact on rice and wheat growth parameter, increased nutrient accessibility, and also benefits the plant health. Numerous studies have been reported that consortium application of bacteria efficiently increased the plant growth parameters and productivity of rice (Lavakusha et al. 2014; Bisht and Chauhan 2020; Ríos-Ruiz et al. 2020) and wheat (Otanga et al. 2018; Wang et al. 2020). In this study, height of plant was significantly higher in all consortia treated plants of rice and wheat under field conditions over non-inoculated plants. Several studies stated that combined application of PGPB have more positive effect on plant height over uninoculated control (Jha et al. 2010; Abbasi et al. 2011; Kumar et al. 2014a, b; Yasmin et al. 2016). In response to application of bacterial consortia, an increase of productive tillers, panicle/spike length, test weight, harvest index, grain yield and straw yield was noticed. The results of Naureen et al. (2015) revealed that most of the individual inoculants significantly augment the yield and yield-related traits, and when four bacterial inoculants used in a consortium (Aeromonas hydrophila BPS10, Bacillus cereus Z2-7, Enterobacter sp. B41 strain SPR7, Enterobacter sp. BPS12) produced a better synergistic effect on plant growth. In our study, the average higher rice–wheat grain (6.84 ton/ha, 6.96 ton/ha) and straw yield (6.09, 6.25 ton/ha) was obtained in the consortia of O. anthropi DPC9 + P. palleroniana DPB13 + P. palleroniana DPB15 + P. fluorescens DPB16 (T7) treated plants. Kumar et al. (2014a, b) also observed that consortium application of A. chlorophenolicus + B. megaterium + Enterobacter significantly increased test weight (17.6%), grain yield (27.5%) and straw yield (29.5%) of wheat under field conditions. Turan et al. (2012) also reported that mixed inoculation of OSU-142 (Bacillus subtilis), M3 (B. megaterium), or Sp245 (Azospirillum brasilense) significantly increased grain yield (33.0%) relative to untreated control plants.
The results obtained with respect to correlation study among rice–wheat yield and yield components are in agreement with those of several other researchers who reported that positive and significant correlation of grain yield with number of tillers, test weight, panicle/spike length, number of grains per panicle/spike and harvest index (Khaliq et al. 2004, Yogameenakshi et al. 2004; Ajmal et al. 2009; Akhtar et al. 2013; Dhurai et al. 2016). Path coefficient analysis of rice revealed that greater positive effect on grain yield are possessed by grains/panicle and total tillers followed by plant height and straw yield. This indicates that more filled grains in panicle are highly reliable component of grain yield. Another important character with high direct effect on grain yield is harvest index followed by panicle length and 1000 grain weight which showed direct effect on grain yield. The direct positive effects of various characters on grain yield observed in the present study are in agreements with the findings of Madhavilatha et al. (2005), Reddy et al. (2013), Basavaraja et al. (2011) and Ratna et al. (2015). In case of wheat direct and indirect effect of spike length, grains per spike, 1000 grain weight, straw yield and harvest index on grain yield was positive, while the direct and indirect effect of plant height and tillers on grain yield was negative. This study indicates that 1000 grain weight and straw yield possessed the highest positive effect on grain yield followed by spike length and tillers. Study of Ahmad et al. (2003), Khokhar et al. (2010), Iftikhar et al. (2012) and Khan et al. (2013) supports the present findings. Hence, harvest index, test weight, straw yield and panicle or spike length should be given prior attention in rice and wheat improvement program because of their major influence on yield.
The obtained results indicated that application of rice and wheat with bacterial consortia improved the nutrient contents under field conditions. The higher NPK content was found in the consortium inoculation of treatment T7-treated plant of both rice and wheat crops as compared to untreated control plants. Our result, with respect to NPK strongly supports the study of Kalita et al. (2015) and Rana et al. (2015) who revealed that bacterial consortia showed higher nutrient uptake than the non-inoculated plants. PGPB inoculants in our study showed multiple PGP characteristic (phosphorus solubilization, siderophore, IAA, NH3 and production), which facilitate rice and wheat plant growth, thereby enhancing the accessibility of nutrients. The compatible nature of bacterial strains used in the present study has shown the synergistic interactions. The inoculation of rice and wheat seeds with treatment T7-exhibited maximum phosphorus content as compared to other treatment over untreated control since all strains in this combination are P-solubilizers might be a reason of increased content of phosphate. Moreover, PGPR produces the antifungal metabolites such as siderophores, antibiotics and hydrolytic enzymes, these metabolites protect plants from pathogen (Chowdhury et al. 2015). Hence, PGPR could be exploited as substitute to the synthetic chemical fertilizers and serve as a viable tool for sustainable agriculture. This argument is strongly supported by previous reports where PGPR inoculation has resulted in the vigorous plant growth, improved nutrition and high productivity of crops (El-Sayed et al. 2014; Majeed et al. 2015). Therefore, inoculation with a consortium of several bacterial strains could be an alternative to inoculation with individual strains, likely reflecting the different mechanisms used by each strain in the consortium.
Conclusion
This study has shown that bacterial consortium inoculation having ACC deaminase activity and other plant growth-promoting attributes augmented rice–wheat growth and grain yield and also enhanced the nutrient availability of plants (Fig. 3). The most promising results were obtained in the consortium application of DPC9 (O. anthropi) + DPB13 (P. palleroniana) + DPB15 (P. palleroniana) + DPB16 (P. fluorescens) that could be used as a potential biofertilizers and a promising option for sustainable agriculture.
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This work was financed by AISRF supported by the Governments of India and Australia. This study was also partially supported by an Indo-Philippines collaboration project.
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This research was supported by Department of Biotechnology.
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Chandra, D., Sharma, A.K. Field evaluation of consortium of bacterial inoculants producing ACC deaminase on growth, nutrients and yield components of rice and wheat. J. Crop Sci. Biotechnol. 24, 293–305 (2021). https://doi.org/10.1007/s12892-020-00077-y
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DOI: https://doi.org/10.1007/s12892-020-00077-y