Exploring Crop–Microbiome Interactions Towards Improving Symbiotic Performance of Chickpea (Cicer arietinum) Cultivars Using Cyanobacterial Inoculants

Simranjit Kaur1, Kunal Ranjan1, Radha Prasanna1, B. Ramakrishnan2, Amrita Kanchan1, Yashbir Singh Shivay3
1Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India
2Division of Microbiology, ICAR–Indian Agricultural Research Institute, New Delhi, India
3Division of Agronomy, ICAR- Indian Agricultural Research Institute, New Delhi, India

Tóm tắt

Từ khóa


Tài liệu tham khảo

Adak A, Prasanna R, Babu S, Bidyarani N, Verma S, Pal M, Shivay YS, Nain L (2016) Micronutrient enrichment mediated by plant-microbe interactions and rice cultivation practices. J Plant Nutr 39:1216–1232

Appleby CA, Bergersen FJ (1980) In: Bergersen FJ (ed) Methods for evaluating biological nitrogen fixation. Wiley, New York

Arefian M, Vessal S, Shafaroudi SM, Bagheri A (2017) Comparative analysis of the reaction to salinity of different chickpea (Cicer aretinum L.) genotypes: a biochemical, enzymatic and transcriptional study. J Plant Growth Regul. https://doi.org/10.1007/s00344-017-9737-z

Arnon DI (1949) Copper enzymes in isolated chloroplasts, polyphenoxidase in Beta vulgaris. Plant Physiol 24:1–15

Arrese-Igor C, Garcia-Plazaola JI, Hernandez A, Aparicio-Tejo PM (1990) Effect of low nitrate supply to nodulated lucerne on time course of activities of enzymes involved in inorganic nitrogen metabolism. Physiol Plant 80:185–190

Babu S, Bidyarani N, Chopra P, Monga D, Kumar R, Prasanna R, Kranthi S, Adak A, Saxena AK (2015) Evaluating microbe-plant interactions and varietal differences for enhancing biocontrol efficacy in root rot challenged cotton crop. Eur J Plant Pathol 142:345–362

Baral B, da Silva JAT, Gupta VN (2014) Xylem-mediated channeling of nitrogen in broad bean (Vicia faba). Environ Exp Biol 12:187–197

Barea JM (2015) Future challenges and perspectives for applying microbial biotechnology in sustainable agriculture based on a better understanding of plant-microbiome interactions. J Soil Sci Plant Nutr 15:261–282

Barnett JP, Millard A, Ksibe AZ, Scanlan DJ, Schmid R, Blindaue CA (2012) Mining genomes of marine cyanobacteria for elements of zinc homeostasis. Front Microbiol 3:142–147

Berkum PV, Sloger C, Weber DF, Cregan PB, Keyser HH (1985) Relationship between ureide N and N2 Fixation, above ground N accumulation, acetylene reduction, and nodule mass in greenhouse and field studies with Glycine max L. (Merr). Plant Physiol 77:53–58

Bidyarani N, Prasanna R, Babu S, Hossain F, Saxena AK (2016) Enhancement of plant growth and yields in chickpea (Cicer arietinum L.) through novel cyanobacterial and biofilmed inoculants. Microbiol Res 188:97–105

Casida LE, Klein DA, Santoro T (1964) Soil dehydrogenase activity. Soil Sci 98:371–376

Chamber-Pérez MA, Camacho-Martínez M, Soriano-Niebla JJ (1997) Nitrate reductase activities of Bradyrhizobium spp. in tropical legumes: effects of nitrate on O2 diffusion in nodules and carbon costs of N2 fixation. J Plant Physiol 150:92–96

Chamizo-Ampudia A, Sanz-Luque E, Llamas A, Galvan A, Fernandez E (2017) Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci 22:163–174

Crawford NM, Kahn ML, Leustek T, Long SR (2000) Nitrogen and sulfur. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry & molecular biology of plants, American Society of Plant Physiologists, Rockville, MD, pp. 786–849

Das K, Rajawat MVS, Saxena AK, Prasanna R (2017) Development of Mesorhizobium ciceri -based biofilms and analyses of their antifungal and plant growth promoting activity in chickpea challenged by Fusarium wilt. Indian J Microbiol 57(1):48–59. https://doi.org/10.1007/s12088-016-0610-8

Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867

de Bruijn FJ (2015) Biological nitrogen fixation. In: Lugtenberg B (ed) Principles of plant-microbe, Springer, Heidelberg, pp. 215-224

De Philippis R, Sili C, Paperi R, Vincenzini M (2001) Exopolysaccharide producing cyanobacteria and their possible exploitation: a review. J Appl Phycol 13:293–299

Deroche M-E, Carrayol E (1988) Nodule phosphoenolpyruvate carboxylase: a review. Physiol Plantar 74(13):775–782. https://doi.org/10.1111/j.1399-3054.1988.tb02051.x

Dey SK, Chakrabarti B, Prasanna R, Pratap D, Singh SD, Purakayastha TJ, Pathak H (2017) Elevated carbon dioxide level along with phosphorus application and cyanobacterial inoculation enhances nitrogen fixation and uptake in cowpea crop. Arch Agron Soil Sci, 63(13):1927–1937 doi: https://doi.org/10.1080/03650340.2017.1315105

Elkoca E, Kocli T, Gunes A, Turan M (2015) The symbiotic performance and plant nutrient uptake of certain nationally registered chickpea (Cicer arietinum L.) cultivars of Turkey. J Plant Nutr 38:1427–1443. https://doi.org/10.1080/01904167.2014.983123

Esfahani MN, Sulieman S, Schulze J, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-S (2014) Approaches for enhancement of N2 fixation efficiency of chickpea (Cicer arietinum L.) under limiting nitrogen conditions. Plant Biotechnol J 12:387–397

FAOSTAT (2014) Agriculture. Available from http://faostat.fao.org

Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120

Flemetakis E, Dimou M, Cotzur D, Aivalakis G, Efrose RC, Kenoutis C, Udvardi M, Katinakis PA (2003) Lotus japonicus β-type carbonic anhydrase gene expression pattern suggests distinct physiological roles during nodule development. Biochim Biophys Acta 1628:186–194

Gan YT, Warkentin TD, McDonald CL, Zentner RP, Vandenberg A (2009) Seed yield and yield stability of chickpea in response to cropping systems and soil fertility in northern latitudes. Agron J 101:1113–1122

Garg N, Singla R (2004) Growth, photosynthesis, nodule nitrogen and carbon fixation in the chickpea cultivars under salt stress. Braz J Plant Physiol 16:137–146

Gaur YD, Sen AN (1981) Cultural and biochemical characteristics of root nodule bacteria of chickpea (Cicer arietinum L.). Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. Zweite Naturwissenschaftliche Abteilung: Mikrobiologie der Landwirtschaft, der Technologie und des Umweltschuzes 136:307–316

Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, Varshney R (2015) The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. Springer Plus 4:31

Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877

Gupta V, Natarajan C, Kumar K, Prasanna R (2011) Identification and characterization of endoglucanases for fungicidal activity in Anabaena laxa (Cyanobacteria). J Appl Phycol 23:73–81

Gupta V, Ratha SK, Sood A, Chaudhary V, Prasanna R (2013) New insights into the biodiversity and applications of cyanobacteria (blue-green algae) – prospects and challenges. Algal Res 2:69–97

Haque M, Hamid A, Bhuiyan NI (2001) Nutrient uptake and productivity as affected by nitrogen and potassium application levels N maize/sweet potato intercropping system. Korean J Crop Sci 46:1–5

Hardy RWF, Burns RC, Holsten RD (1973) Application of the acetylene-ethylene assay for measurements of nitrogen fixation. Soil Biol Biochem 5:47–81. https://doi.org/10.1016/0038-0717(73)90093-X

Hegazi AZ, Mostafa MSS, Ahmed HMI (2010) Influence of different cyanobacterial application methods on growth and seed production of common bean under various levels of mineral nitrogen fertilization. Nat Sci 8:183–194

Herridge DF, Bergersen FJ, Peoples MB (1990) Measurement of nitrogen fixation by soybean in the field using the ureide and natural 15N abundance methods. Plant Physiol 98:708–716

Hesse PR (1971) A textbook of soil chemical analysis. John Murray, London

Hirsch PR, Mauchline TH, Clark IM (2013) Culture-independent molecular approaches to microbial ecology in soil and the rhizosphere. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1. Wiley Blackwell, Hoboken, pp. 45–55

Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

Israr D, Mustafa G, Khan KS, Shahzad M, Ahmad N, Masood S (2016) Interactive effects of phosphorus and Pseudomonas putida on chickpea (Cicer arietinum L.) growth, nutrient uptake, antioxidant enzymes and organic acids exudation. Plant Physiol Biochem 108:304–312

Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44

Juge C, Prévost D, Bertrand A, Bipfubusa M, Chalifour F-P (2012) Growth and biochemical responses of soybean to double and triple microbial associations with Bradyrhizobium, Azospirillum and arbuscular mycorrhizae. Appl Soil Ecol 61:147–157

Karthikeyan N, Prasanna R, Nain L, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur J Soil Biol 43:23–30

Kaur S, Khanna V (2014) Effect of temperature-tolerant rhizobial isolates as PGPR on nodulation, growth and yield of pigeonpea [Cajanus cajan (L) Milsp.]. J Food Legumes 26:80–83

Kumar M, Prasanna R, Bidyarani N, Babu S, Mishra BK, Kumar A, Adak A, Jauhari S, Yadav K, Singh R, Saxena AK (2013) Evaluating the plant growth promoting ability of thermotolerant bacteria and cyanobacteria and their interactions with seed spice crops. Sci Hortic 164:94–101

Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am 42:421–428

Lowe RH, Evans HJ (1964) Preparation and some properties of a soluble nitrate reductase from Rhizobium japonicum. ‎Biochim Biophys Acta 85:377–389

Mackinney G (1941) Absorption of light by chlorophyll. J Biol Chem 140:315–323

Nunan N, Morgan MA, Herlihy M (1998) Ultraviolet absorbance (280 nm) of compounds released from soil during chloroform fumigation as an estimate of the microbial biomass. Soil Biol Biochem 30:599–1603

Olsen S, Cole C, Watanabe F, Dean L (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular Nr 939, US Gov. Print. Office, Washington, D.C.

Olsson MO, Falkengren-Grerup U (2000) Potential nitrification as an indicator of preferential uptake of ammonium or nitrate by plants in an oak woodland understory. Ann Bot 85:299–305

Patel D, Jha CK, Tank N, Saraf M (2012) Growth enhancement of chickpea in saline soils using plant growth promoting rhizobacteria. J Plant Growth Regul 31:53–62

Peoples MB, Herridge DF (1990) Nitrogen fixation by legumes in tropical and sub-tropical agriculture. Adv Agron 44:155–223

Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103

Prasad R, Shivay YS, Kumar D, Sharma SN (2006) Learning by doing exercises in soil fertility. Division of Agronomy, Indian Agricultural Research Institute, New Delhi

Prasanna R, Pattnayak S, Sugitha TCK, Nain L, Saxena AK (2011) Development of cyanobacterium based biofilms and their in vitro evaluation for agriculturally useful traits. Folia Microbiol 56:49–58

Prasanna R, Kumar A, Babu S, Chawla G et al (2013) Deciphering the biochemical spectrum of novel cyanobacterium-based biofilms for use as inoculants. Biol Agric Hortic 29:145–158

Prasanna R, Sood A, Ratha SK, Singh PK (2014a) Cyanobacteria as a “green option” for sustainable agriculture. In: Sharma NK, Stal LJ, Rai AK (eds) Cyanobacteria: an economic perspective, Wiley, Chichester, pp 145–166

Prasanna R, Triveni S, Bidyarani N, Babu S, Yadav K, Adak A, Khetarpal S, Pal M, Shivay YS, Saxena AK (2014b) Evaluating the efficacy of cyanobacterial formulations and biofilmed inoculants for leguminous crops. Arch Agron Soil Sci 60:349–366

Prasanna R, Ramakrishnan B, Simranjit K, Ranjan K, Kanchan A, Hossain F, Nain L (2017) Cyanobacterial and rhizobial inoculation modulates the plant physiological attributes and nodule microbial communities of chickpea. Arch Microbiol 199(9):1311–1323. https://doi.org/10.1007/s00203-017-1405-y

Priya H, Prasanna R, Ramakrishnan B, Bidyarani N, Babu S, Thapa S, Renuka N (2015) Influence of cyanobacterial inoculation on the culturable microbiome and growth of rice. Microbiol Res 171:78–89

Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531

Ramakrishnan B, Kaur S, Prasanna R, Ranjan K, Kanchan A, Hossain F, Shivay Y, Nain L (2017) Microbial inoculation of seeds characteristically shapes the rhizosphere microbiome in desi and kabuli chickpea types. J Soils Sediments. https://doi.org/10.1007/s11368-017-1685-5

Ranjan K, Priya H, Ramakrishnan B, Prasanna R, Venkatachalam S, Thapa S, Tiwari R, Nain L, Singh R, Shivay YS (2016) Cyanobacterial inoculation modifies the rhizosphere microbiome of rice planted to a tropical alluvial soil. Appl Soil Ecol 108:195–203

Renuka N, Prasanna R, Sood A, Bansal R, Singh R, Shivay YS, Nain L, Ahluwalia AS (2017) Wastewater grown microalgal biomass as inoculants for improving micronutrient availability in wheat. Rhizosphere 3:150–159

Rupela OP, Saxena MC (1987) Nodulation and nitrogen fixation in chickpea. In: Saxena MC, Singh KB (eds) The chickpea. CAB International, Wallingford, pp 191–206

Saini R, Dudeja SS, Giri R, Kumar V (2015) Isolation, characterization, and evaluation of bacterial root and nodule endophytes from chickpea cultivated in Northern India. J Basic Microbiol 55:74–81

Salazar S, Sánchez LE, Alvarez J, Valverde A, Galindo P, Igual JM, Peix A, Santa-Regina I (2011) Correlation among soil enzyme activities under different forest system management practices. Ecol Eng 37:1123–1131

Singh JS, Pandey VC, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agric Ecosyst Environ 140:339–353

Singh JS, Kumar A, Rai AN, Singh DP (2016) Cyanobacteria: a precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front Microbiol. https://doi.org/10.3389/fmicb.2016.00529

Singh D, Geat N, Rajawat MVS, Mahajan MM, Prasanna R, Singh S, Kaushik R, Singh RN, Kumar K, Saxena AK (2018) Deciphering the mechanisms of endophyte-mediated biofortification of Fe and Zn in wheat. J Plant Growth Regul 37:174–182

Soussi M, Lluch C, Ocana A (1999) Comparative study of nitrogen fixation and carbon metabolism in two chickpea (Cicer arietinum L.) cultivars under salt stress. J Exp Bot 50:1701–1708

Subbiah BV, Asija GL (1956) A rapid procedure for the determination of available nitrogen in soils. Curr Sci 25:259–260

Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072

Tilak KVBR, Ranganayaki N, Pal KK, De R, Saxena AK, Shekhar NC, Mittal S, Tripathi AK, Johri BN (2005) Diversity of plant growth and soil health supporting bacteria. Curr Sci 89:136–150

Tomaszewska B, Marczewski W, Schramm RW (1983) Phosphoenolpyruvate carboxylase in the roots of yellow lupin (Lupinus luteus). Acta Biochim Polon 30:265–275

Yadav J, Verma JP (2014) Effect of seed inoculation with indigenous Rhizobium and plant growth promoting rhizobacteria on nutrients uptake and yields of chickpea (Cicer arietinum L.). Eur J Soil Biol 63:70–77

Zhang N, He XD, Gao YB, Li YH, Wang HT, Ma D, Zhang R, Yang S (2010) Pedogenic carbonate and soil dehydrogenase activity in response to soil organic matter in Artemisia ordosica community. Pedosphere 20:229–235