Improving Strategic Growth Stage-based Drought Tolerance in Quinoa by Rhizobacterial Inoculation

ABSTRACT Climate change is imposing high temperature resulting in prolonged drought episodes and shrinking of fresh water resources across the globe. In this scenario, even drought tolerant crops like quinoa are also losing significant yield. However, this study was planned to investigate the impact of drought on quinoa at critical growth stages and bacterial inoculation to improve drought tolerance. Drought was imposed by maintaining 25% pot water holding capacity (PWC) at multiple leaf, flowering, and seed filling stage (DSFS), while 80% PWC was considered as control. Three strains of plant growth promoting rhizobacteria (PGPR) named as: Bacillus licheniformis, Pseudomonas fluorescens, and Azospirillum brasilense were inoculated with quinoa seeds before sowing with respect to drought treatments. PGPR inoculation mitigated the drastic effects of drought by improving crop growth, net assimilation rate, water use efficiency, leaf chlorophyll, and phenolic contents, all of these ultimately contributed to improvement in grain yield and its contributing attributes. Moreover, PGPR markedly improves the grain quality attributes including protein, phosphorus, and potassium contents. Principal component analysis linked the different scales of study and demonstrated the potential of physio-biochemical traits to explain the quinoa yield variations under drought condition with response to PGPR inoculation. Among different PGPR, A. brasilense was found most effective both under normal and drought conditions. Overall, DSFS has more detrimental effects among critical growth stages of quinoa and A. brasilense can be used as a shotgun tactic to ameliorate drought stress in quinoa.

[1]  M. Saleem,et al.  Effect of rhizobacteria and cytokinins application on wheat growth and yield under normal vs drought conditions , 2019, Communications in Soil Science and Plant Analysis.

[2]  M. Saleem,et al.  Investigating the effect of Azospirillum brasilense and Rhizobium pisi on agronomic traits of wheat (Triticum aestivum L.) , 2019, Archives of Agronomy and Soil Science.

[3]  R. Kaushal,et al.  Effect of Indigenous Plant Growth-Promoting Rhizobacteria on Wheat (Triticum Aestivum L.) Productivity and Soil Nutrients , 2018, Communications in Soil Science and Plant Analysis.

[4]  Hassan Iqbal,et al.  Hydrogen peroxide application improves quinoa performance by affecting physiological and biochemical mechanisms under water‐deficit conditions , 2018 .

[5]  Hassan Iqbal,et al.  Differential response of quinoa genotypes to drought and foliage-applied H2O2 in relation to oxidative damage, osmotic adjustment and antioxidant capacity. , 2018, Ecotoxicology and environmental safety.

[6]  N. Khan,et al.  Impact of Salicylic Acid and PGPR on the Drought Tolerance and Phytoremediation Potential of Helianthus annus , 2018, Front. Microbiol..

[7]  Hassan Iqbal,et al.  Soil drenching of paclobutrazol: An efficient way to improve quinoa performance under salinity. , 2018, Physiologia plantarum.

[8]  M. Saleem,et al.  Amelioration in Growth and Physiological Efficiency of Sunflower (Helianthus annuus L.) under Drought by Potassium Application , 2018, Communications in Soil Science and Plant Analysis.

[9]  M. Hungria,et al.  Azospirillum: benefits that go far beyond biological nitrogen fixation , 2018, AMB Express.

[10]  D. Watts,et al.  Influence of Plant Growth-Promoting Rhizobacteria on Corn Growth Under Different Fertility Sources , 2018 .

[11]  A. Nawaz,et al.  Foliage‐applied sodium nitroprusside and hydrogen peroxide improves resistance against terminal drought in bread wheat , 2017 .

[12]  Dalel Chakri Telahigue,et al.  Grain yield, biomass productivity and water use efficiency in quinoa (Chenopodium quinoa Willd.) under drought stress , 2017 .

[13]  V. Sosa‐Zuniga,et al.  Phenological growth stages of quinoa (Chenopodium quinoa) based on the BBCH scale , 2017 .

[14]  J. Coimbra,et al.  Quinoa: Nutritional, functional, and antinutritional aspects , 2017, Critical reviews in food science and nutrition.

[15]  Ş. Kuşvuran,et al.  Effects of drought stress on physiological and biochemical changes in Phaseolus vulgaris L. , 2017 .

[16]  S. Jacobsen,et al.  Growth and Physiological Responses of Quinoa to Drought and Temperature Stress , 2016 .

[17]  Sandhya Vardharajula,et al.  Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. , 2016, Microbiological research.

[18]  S. Roura,et al.  Azospirillum inoculation effects on growth, product quality and storage life of lettuce plants grown under salt stress , 2015 .

[19]  J. Vanderleyden,et al.  Auxin Signaling in Azospirillum brasilense: A Proteome Analysis , 2015 .

[20]  R. Ragab,et al.  Physiological and photosynthetic response of quinoa to drought stress , 2015 .

[21]  Ali Reza Sepaskhah,et al.  Effect of different saline groundwater depths and irrigation water salinities on yield and water use of quinoa in lysimeter , 2015 .

[22]  E. M. Souza,et al.  Use of nitrogen-fixing bacteria to improve agricultural productivity , 2014, BMC Proceedings.

[23]  A. Maleki,et al.  The Co-application of Plant Growth Promoting Rhizobacteria and Inoculation with Rhizobium Bacteria on Grain Yield and Its Components of Mungbean (Vigna radiate L.) in Ilam Province, Iran , 2014 .

[24]  M. Riccardi,et al.  Growth and Ionic Content of Quinoa Under Saline Irrigation , 2014 .

[25]  J. Hasanpour,et al.  Effect of Selenium Spraying on Yield and Growth Indices of Wheat (Triticum Aestivum L.) Under Drought Stress Condition , 2014 .

[26]  M. Rehmani,et al.  Yield and quality responses of two indica rice hybrids to post-anthesis asymmetric day and night open-field warming in lower reaches of Yangtze River delta , 2014 .

[27]  K. Msaada,et al.  Effect of drought on safflower natural dyes and their biological activities , 2014, EXCLI journal.

[28]  A. Bano,et al.  Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize , 2014 .

[29]  Jong-Hui Lim,et al.  Induction of Drought Stress Resistance by Multi-Functional PGPR Bacillus licheniformis K11 in Pepper , 2013, The plant pathology journal.

[30]  J. Verma,et al.  Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture , 2013 .

[31]  N. Arora,et al.  Integrated approach for disease management and growth enhancement of Sesamum indicum L. utilizing Azotobacterchroococcum TRA2 and chemical fertilizer , 2012, World journal of microbiology & biotechnology.

[32]  Babu Joseph,et al.  Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.) , 2012 .

[33]  F. Prado,et al.  Interrelationships among seed yield, total protein and amino acid composition of ten quinoa (Chenopodium quinoa) cultivars from two different agroecological regions. , 2012, Journal of the science of food and agriculture.

[34]  F. Nawaz,et al.  NUTRIENT UPTAKE, PHYSIOLOGICAL RESPONSES, AND YIELD ATTRIBUTES OF WHEAT (TRITICUM AESTIVUM L.) EXPOSED TO EARLY AND LATE DROUGHT STRESS , 2012 .

[35]  R. Rodriguez,et al.  Increased Fitness of Rice Plants to Abiotic Stress Via Habitat Adapted Symbiosis: A Strategy for Mitigating Impacts of Climate Change , 2011, PloS one.

[36]  B. Venkateswarlu,et al.  Role of microorganisms in adaptation of agriculture crops to abiotic stresses , 2011 .

[37]  C. Kammann,et al.  Influence of biochar on drought tolerance of Chenopodium quinoa Willd and on soil–plant relations , 2011, Plant and Soil.

[38]  K. Ahmad,et al.  THE EFFECT OF PLANT GROWTH PROMOTING RHIZOBACTERIA ON MACRO ELEMENT CONTENT AND YIELD OF ALOE VERA IN GREEN HOUSE CONDITIONS , 2011 .

[39]  S. Alamri,et al.  Effect of nitrogen supply and Azospirillum brasilense Sp-248 on the response of wheat to seawater irrigation. , 2009, Saudi journal of biological sciences.

[40]  S. Jacobsen,et al.  Does root-sourced ABA play a role for regulation of stomata under drought in quinoa (Chenopodium quinoa Willd.). , 2009 .

[41]  M. Farooq,et al.  Improving the Drought Tolerance in Rice (Oryza sativa L.) by Exogenous Application of Salicylic Acid , 2009 .

[42]  S. Dhondt,et al.  Gibberellin Signaling Controls Cell Proliferation Rate in Arabidopsis , 2009, Current Biology.

[43]  Xiaodong Yan,et al.  Climate change and drought: a risk assessment of crop-yield impacts. , 2009 .

[44]  M. Farooq,et al.  Exogenous Glycinebetaine and Salicylic Acid Application Improves Water Relations, Allometry and Quality of Hybrid Sunflower under Water Deficit Conditions , 2009 .

[45]  C. Prigent-Combaret,et al.  Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclopropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other Proteobacteria. , 2008, FEMS microbiology ecology.

[46]  C. A. Jaleel,et al.  Osmoregulation and antioxidant metabolism in drought-stressed Helianthus annuus under triadimefon drenching. , 2008, Comptes rendus biologies.

[47]  D. Raes,et al.  Introducing deficit irrigation to stabilize yields of quinoa (Chenopodium quinoa Willd.) , 2008 .

[48]  Kuan-Hung Lin,et al.  The Effects of Flooding and Drought Stresses on the Antioxidant Constituents in Sweet Potato Leaves , 2006 .

[49]  S. Herbert,et al.  Interaction Between Phosphorus Nutrition and Drought on Grain Yield, and Assimilation of Phosphorus and Nitrogen in Two Soybean Cultivars Differing in Protein Concentration in Grains , 2006 .

[50]  Fengmin Li,et al.  Yield performance of spring wheat improved by regulated deficit irrigation in an arid area , 2006 .

[51]  C. Barassi,et al.  Water relations and yield in Azospirillum-inoculated wheat exposed to drought in the field , 2004 .

[52]  Andrew L. Waterhouse,et al.  Determination of Total Phenolics , 2003 .

[53]  S. Jacobsen,et al.  Nutritional Value and Use of the Andean Crops Quinoa (Chenopodium quinoa) and Kañiwa (Chenopodium pallidicaule) , 2003 .

[54]  M. Andersen,et al.  Leaf gas exchange and water relation characteristics of field quinoa (Chenopodium quinoa Willd.) during soil drying , 2000 .

[55]  Shu Fukai,et al.  Phenology in rainfed lowland rice , 1999 .

[56]  R. Stott,et al.  The World Bank , 2008, Annals of tropical medicine and parasitology.

[57]  G. J. Mitchell,et al.  Principles and procedures of statistics: A biometrical approach , 1981 .

[58]  James H. Torrie,et al.  Principles and procedures of statistics: a biometrical approach (2nd ed) , 1980 .

[59]  M. Pontin,et al.  Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. , 2015, Physiologia plantarum.

[60]  M. Valizadeh,et al.  Proline, glycine betaine, total phenolics and pigment contents in response to osmotic stress in maize seedlings , 2015 .

[61]  M. Heidari,et al.  Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.) , 2012 .

[62]  S. Burdman,et al.  Key physiological properties contributing to rhizosphere adaptation and plant growth promotion abilities of Azospirillum brasilense. , 2012, FEMS microbiology letters.

[63]  C. Ryu,et al.  Rhizosphere bacteria help plants tolerate abiotic stress. , 2009, Trends in plant science.

[64]  G. Murtaza,et al.  YIELD STABILITY ANALYSIS CONFERRING ADAPTATION OF WHEAT TO PRE- AND POST-ANTHESIS DROUGHT CONDITIONS , 2007 .

[65]  P. Hasegawa,et al.  Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops , 2007 .

[66]  N. Anten.  Plant ecology.Schulze ED, Beck E, Müller-Hohenstein K. 2005. Berlin/Heidelberg: Springer. $89·95 (hardback). 702 pp. , 2006 .

[67]  D. Raes,et al.  Response of quinoa (Chenopodium quinoa Willd.) to differential drought stress in the Bolivian Altiplano: Towards a deficit irrigation strategy within a water scarce region , 2006 .

[68]  N. Samarah.  Effects of drought stress on growth and yield of barley , 2005 .

[69]  B. Lugtenberg,et al.  Molecular determinants of rhizosphere colonization by Pseudomonas. , 2001, Annual review of phytopathology.

[70]  Kenneth Helrick,et al.  Official methods of analysis , 1990 .