Abstract
Legumes are an indispensable food after cereals with extensive production across the world. Legume production is imposed with limitations and has been augmented by various environmental stresses. The symbiotic relations between legumes and rhizobacteria have been an intriguing topic of research in view of their roles in plant growth, development and various stress responses. Recent advances in gene networks involving a plethora of evolutionarily conserved miRNAs have been investigated pertaining to their roles in plant stress responses. The interaction between plant growth-promoting rhizobacteria (PGPR) strain Pseudomonas putida (RA), MTCC5279 and abiotic stress-responsive miRNAs have previously been studied with roles in abiotic stress mitigation by modulating stress-responsive miRNAs and their target genes. The present study is an investigation involving the role of RA-responsive miR166 for drought mitigation in desi chickpea genotype. Drought-stressed chickpea plants when inoculated with RA, the inverse correlation in expression patterns were noticed in miR166 and its validated target, ATHB15. miR166-directed cleavage of ATHB15 has been carried out in drought-treated plantlets upon RA inoculation using 5´RLM-RACE analysis. Tissue-specific expression patterns in 15 days old chickpea seedlings including leaves, shoot and roots when exposed to salinity, drought and abscisic acid at different time points indicating the role of miR166 in different abiotic stress responses. In view of the results, validation and functional characterization of such interactions involving stress-responsive miRNAs along with microbial applications in stress management could be an important method for crop improvement.
Key message
Overexpression of Pseudomonas putida RA-responsive microRNA166 in chickpea reveals its important role in beneficial plant-root rhizobacteria interaction by conferring drought stress tolerance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
No data available.
References
Akdogan G, Tufekci ED, Uranbey S, Unver T (2016) miRNA-based drought regulation in wheat. Funct Integr Genomics 16:221–233
Alam P, Albalawi TH (2020) In vitro alteration of artemisinin biosynthesis in Artemisia annua L. during treatment with methyl jasmonate. Trop J Pharm Res 19:33–37. https://doi.org/10.4314/tjpr.v19i1.5
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428. https://doi.org/10.1071/BI9620413
Bhushan D, Pandey A, Choudhary MK, Datta A, Chakraborty S, Chakraborty N (2007) Comparative proteomics analysis of differentially expressed proteins in chickpea extracellular matrix during dehydration stress. Mol Cell Proteomics 6:1868–1884. https://doi.org/10.1074/mcp.M700015-MCP200
Boualem A, Laporte P, Jovanovic M, Laffont C, PletJ CJP, Niebel A, Crespi M, Frugier F (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54:876–887. https://doi.org/10.1111/j.1365-313X.2008.03448.x
Bresson J, Varoquaux F, Bontpart T, Touraine B, Vile D (2013) The PGPR strain P hyllobacterium brassicacearum STM 196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytol 200:558–569. https://doi.org/10.1111/nph.12383
Carillo P, Gibon Y (2011) Protocol: extraction and determination of proline. PrometheusWiki
Çelik Ö, Akdaş EY (2019) Tissue-specific transcriptional regulation of seven heavy metal stress-responsive miRNAs and their putative targets in nickel indicator castor bean (R. communis L.) plants. Ecotoxicol Environ Saf 170:682–690. https://doi.org/10.1016/j.ecoenv.2018.12.006
Cha-um S, Yamada N, Takabe T, Kirdmanee C (2013) Physiological features and growth characters of oil palm (Elaeis guineensis Jacq.) in response to reduced water-deficit and rewatering. Aust J Crop Sci 7:432
Chen X, Chen Z, Zhao H, Zhao Y, Cheng B, Xiang Y (2014) Genome-wide analysis of soybean HD-Zip gene family and expression profiling under salinity and drought treatments. PLoS ONE 9:87156. https://doi.org/10.1371/journal.pone.0087156
Devasirvatham V, Tan DK (2018) Impact of high temperature and drought stresses on chickpea production. Agronomy 8:145. https://doi.org/10.3390/agronomy8080145
Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38. https://doi.org/10.1093/aob/mcn205
Ding Y, Tao Y, Zhu C (2013) Emerging roles of microRNAs in the mediation of drought stress response in plants. J Exp Bot 64:3077–3086. https://doi.org/10.1093/jxb/ert164
Ding Y, GongS WY, Wang F, Bao H, Sun J, Cai C, Yi K, Chen Z, Zhu C (2018) MicroRNA166 modulates cadmium tolerance and accumulation in rice. Plant Physiol 177:1691–1703. https://doi.org/10.1104/pp.18.00485
Donaire L, Pedrola L, de la Rosa R, Llave C (2011) High-throughput sequencing of RNA silencing-associated small RNAs in olive (Olea europaea L.). PLoS ONE 6:27916. https://doi.org/10.1371/journal.pone.0027916
Du Q, Wang H (2015) The role of HD-ZIP III transcription factors and miR165/166 in vascular development and secondary cell wall formation. Plant Signal Behav 10:1078955. https://doi.org/10.1080/15592324.2015.1078955
FAOSTAT (2019). https://faostat.fao.org/site/291/default.aspx
Garg R, Sahoo A, Tyagi AK, Jain M (2010) Validation of internal control genes for quantitative gene expression studies in chickpea (Cicer arietinum L.). Biochem Biophys Res Commun 96:283–288. https://doi.org/10.1016/j.bbrc.2010.04.079
Gentile A, Dias LI, Mattos RS, Ferreira TH, Menossi M (2015) MicroRNAs and drought responses in sugarcane. Front Plant Sci 6:58. https://doi.org/10.3389/fpls.2015.00058
Grover M, Madhubala R, Ali SZ, Yadav SK, Venkateswarlu B (2014) Influence of Bacillus spp. strains on seedling growth and physiological parameters of Sorghum under moisture stress conditions. J Basic Microbiol 54:951–961. https://doi.org/10.1002/jobm.201300250
Guo Y, Zhao S, Zhu C, Chang X, Yue C, Wang Z, LinY LZ (2017) Identification of drought-responsive miRNAs and physiological characterization of tea plant (Camellia sinensis L.) under drought stress. BMC Plant Biol 17:1–20
Hajyzadeh M, Turktas M, Khawar KM, Unver T (2015) miR408 overexpression causes increased drought tolerance in chickpea. Gene 555:186–193. https://doi.org/10.1016/j.gene.2014.11.002
Hamza NB, Sharma N, Tripathi A, Sanan-Mishra N (2016) MicroRNA expression profiles in response to drought stress in Sorghum bicolor. Gene Expr Patterns 20:88–98. https://doi.org/10.1016/j.gep.2016.01.001
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23:1986–1997. https://doi.org/10.1101/gad.1819909
Iwamoto M, Tagiri A (2016) Micro RNA-targeted transcription factor gene RDD 1 promotes nutrient ion uptake and accumulation in rice. Plant J 85:466–477. https://doi.org/10.1111/tpj.13117
Jain M, Chevala VN, Garg R (2014) Genome-wide discovery and differential regulation of conserved and novel microRNAs in chickpea via deep sequencing. J Exp Bot 65:5945–5958. https://doi.org/10.1093/jxb/eru333
Jatan R, Chauhan PS, Lata C (2018) Pseudomonas putida modulates the expression of miRNAs and their target genes in response to drought and salt stresses in chickpea (Cicer arietinum L.). Genomics 111:509–519. https://doi.org/10.1016/j.ygeno.2018.01.007
Jatan R, Tiwari S, Asif MH, Lata C (2019) Genome-wide profiling reveals extensive alterations in Pseudomonas putida-mediated miRNAs expression during drought stress in chickpea (Cicer arietinum L.). Environ Exp Bot 157:217–227. https://doi.org/10.1016/j.envexpbot.2018.10.003
Jia X, Ren L, Chen QJ, Li R, Tang G (2009) UV-B-responsive microRNAs in Populus tremula. J Plant Hysiol. 166:2046–2057. https://doi.org/10.1016/j.jplph.2009.06.011
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799. https://doi.org/10.1016/j.molcel.2004.05.027
Kang SM, Khan AL, Waqas M, You YH, Kim JH, Kim JG, Hamayun M, Lee IJ (2014) Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9:673–682. https://doi.org/10.1080/17429145.2014.894587
Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233:471–484
Khan N, Bano A, Zandi P (2018) Effects of exogenously applied plant growth regulators in combination with PGPR on the physiology and root growth of chickpea (Cicer arietinum) and their role in drought tolerance. J Plant Interact 13:239–247. https://doi.org/10.1080/17429145.2018.1471527
Khodadadi M (2013) Effect of drought stress on yield and water relative content in chickpea. IJPP 4:1168–1172
Kim J, Jung JH, Reyes JL, Kim YS, Kim SY, Chung KS, Kim JA, Lee M, Lee Y, Narry Kim V, Chua NH (2005) microRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J 42(84–94):v. https://doi.org/10.1111/j.1365-313X.2005.02354.x
Kitazumi A, Kawahara Y, Onda TS, De Koeyer D, de los Reyes BG, (2015) Implications of miR166 and miR159 induction to the basal response mechanisms of an andigena potato (Solanum tuberosum subsp. andigena) to salinity stress, predicted from network models in Arabidopsis. Genome 58:13–24. https://doi.org/10.1139/gen-2015-0011
Kohli D, Joshi G, Deokar AA, Bhardwaj AR, Agarwal M, Katiyar-Agarwal S, Srinivasan R, Jain PK (2014) Identification and characterization of wilt and salt stress-responsive microRNAs in chickpea through high-throughput sequencing. PLoS ONE 9:108851. https://doi.org/10.1371/journal.pone.0108851
Kramer MF (2011) Stem-loop RT-qPCR for miRNAs. Curr Protocol Mol Biol 95:15–10. https://doi.org/10.1002/0471142727.mb1510s95
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA-X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547. https://doi.org/10.1093/molbev/msy096
Kuruvilla L, Sathik MB, Thomas M, Luke LP, Sumesh KV, Annamalainathan K (2016) Expression of miRNAs of Hevea brasiliensis under drought stress is altered in clones with varying levels of drought tolerance. IJBT 15:153–160
Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748. https://doi.org/10.1093/jxb/err210
Lata C, Muthamilarasan M, Prasad M (2015) Drought stress responses and signal transduction in plants. Elucidation of abiotic stress signaling in plants. Springer, New York, pp 195–225
Li X, Xie X, Li J, Cui Y, Hou Y, Zhai L, Wang X, Fu Y, Liu R, Bian S (2017) Conservation and diversification of the miR166 family in soybean and potential roles of newly identified miR166s. BMC Plant Biol 17:1–18
Li Z, Gao Z, Li R, Xu Y, Kong Y, Zhou G, Meng C, Hu R (2020) Genome-wide identification and expression profiling of HD-ZIP gene family in Medicago truncatula. Genomics 112:3624–3635. https://doi.org/10.1016/j.ygeno.2020.03.008
Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240
Liu Q, Chen YQ (2009) Insights into the mechanism of plant development: interactions of miRNAs pathway with phytohormone response. Biochem Biophys Res Commun 384:1–5. https://doi.org/10.1016/j.bbrc.2009.04.028
Liu WW, Meng J, Cui J, Luan YS (2017) Characterization and function of MicroRNAs in plants. Front Plant Sci 8:2200. https://doi.org/10.3389/fpls.2017.02200
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056. https://doi.org/10.1126/science.1076311
Lopes MS, Araus JL, Van Heerden PD, Foyer CH (2011) Enhancing drought tolerance in C4 crops. J Exp Bot 62:3135–3153. https://doi.org/10.1093/jxb/err105
Luo J, Yu CM, Yan M, Chen YH (2020) Molecular characterization of the promoter of the stress-inducible ZmMYB30 gene in maize. Biol Plant 64:200–210. https://doi.org/10.32615/bp.2020.011
Mandel T, Candela H, Landau U, Asis L, Zelinger E, Carles CC, Williams LE (2016) Differential regulation of meristem size, morphology and organization by the ERECTA, CLAVATA and class III HD-ZIP pathways. Development 143:1612–1622. https://doi.org/10.1242/dev.129973
Millar AA (2020) The function of miRNAs in plants. Plants 9:198. https://doi.org/10.3390/plants9020198
Nautiyal CS, Srivastava S, Chauhan PS, Seem K, Mishra A, Sopory SK (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physio. Biochem 66:1–9. https://doi.org/10.1016/j.plaphy.2013.01.020
Ochando I, Jover-Gil S, Ripoll JJ, Candela H, Vera A, Ponce MR, Martínez-Laborda A, Micol JL (2006) Mutations in the microRNA complementarity site of the INCURVATA4 gene perturb meristem function and adaxialize lateral organs in Arabidopsis. Plant Physiol 141:607–619. https://doi.org/10.1104/pp.106.077149
Ohashi-Ito K, Fukuda H (2003) HD-Zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44:1350–1358. https://doi.org/10.1093/pcp/pcg164
Passricha N, Saifi S, Ansari MW, Tuteja N (2017) Prediction and validation of cis-regulatory elements in 5′ upstream regulatory regions of lectin receptor-like kinase gene family in rice. Protoplasma 254:669–684. https://doi.org/10.1007/s00709-016-0979-6
Pla M, Vilardell J, Guiltinan MJ, Marcotte WR, Niogret MF, Quatrano RS, Pagès M (1993) The cis-regulatory element CCACGTGG is involved in ABA and water-stress responses of the maize gene rab28. Plant Mol Biol 21:259–266
Shah TM, Imran M, Atta BM, Ashraf MY, Hameed A, Waqar I, Shafiq M, Hussain K, Naveed M, Aslam M, Maqbool MA (2020) Selection and screening of drought tolerant high yielding chickpea genotypes based on physio-biochemical indices and multi-environmental yield trials. BMC Plant Biol 20:1–16
Sharma A, Ruiz-Manriquez LM, Serrano-Cano FI, Reyes-Pérez PR, Tovar-Alfaro CK, Barrón Andrade YE, Hernández Aros AK, Srivastava A, Paul S (2020) Identification of microRNAs and their expression in leaf tissues of guava (Psidium guajava L.) under salinity stress. Agronomy 10:1920. https://doi.org/10.3390/agronomy10121920
Shriram V, Kumar V, Devarumath RM, Khare TS, Wani SH (2016) MicroRNAs as potential targets for abiotic stress tolerance in plants. Front Plant Sci 7:817. https://doi.org/10.3389/fpls.2016.00817
Shuai P, Liang D, Zhang Z, Yin W, Xia X (2013) Identification of drought-responsive and novel Populus trichocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis. BMC Genomics 14:1–14
Singh A, Roy S, Singh S, Das SS, Gautam V, Yadav S, Kumar A, Singh A, Samantha S, Sarkar AK (2017) Phytohormonal crosstalk modulates the expression of miR166/165s, target Class III HD-ZIPs, and KANADI genes during root growth in Arabidopsis thaliana. Sci Rep 7:1–13
Srivastava S, Zheng Y, Kudapa H, Jagadeeswaran G, Hivrale V, Varshney RK, Sunkar R (2015) High throughput sequencing of small RNA component of leaves and inflorescence revealed conserved and novel miRNAs as well as phasiRNA loci in chickpea. Plant Sci 35:46–57. https://doi.org/10.1016/j.plantsci.2015.03.002
Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2012) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309. https://doi.org/10.1016/j.tplants.2007.05.001
Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117. https://doi.org/10.1016/j.plaphy.2015.11.001
Tiwari S, Lata C, Singh Chauhan P, Prasad V, Prasad M (2017) A functional genomic perspective on drought signalling and its crosstalk with phytohormone-mediated signalling pathways in plants. Curr Genomics 18:469–482. https://doi.org/10.2174/1389202918666170605083319
Trindade I, Santos D, Dalmay T, Fevereiro P (2011) Facing the environment: small RNAs and the regulation of gene expression under abiotic stress in plants. Abiotic Stress Response Plants Physiol Biochem Genet Pres Shanker a, Venkateswarlu B Eds 113:136
Ullah A, Hussain A, Shaban M, Khan AH, Alariqi M, Gul S, Jun Z, Lin S, Li J, Jin S, Munis MFH (2018) Osmotin: a plant defense tool against biotic and abiotic stresses. Plant Physiol Biochem 123:149–159. https://doi.org/10.1016/j.plaphy.2017.12.012
Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687. https://doi.org/10.1016/j.cell.2009.01.046
Wai AH, Waseem M, Khan ABM, Nath UK, Lee DJ, Kim ST, Kim CK, Chung MY (2021) Genome-wide identification and expression profiling of the PDI gene family reveals their probable involvement in abiotic stress tolerance in tomato (Solanum lycopersicum L.). Genes 12:23. https://doi.org/10.3390/genes12010023
Xia Z, Zhao Z, Li M, Chen L, Jiao Z, Wu Y, Zhou T, Fan YuW, Z, (2018) Identification of miRNAs and their targets in maize in response to Sugarcane mosaic virus infection. Plant Physiol Biochem 125:143–152. https://doi.org/10.1016/j.plaphy.2018.01.031
Xie F, Stewart CN Jr, Taki FA, He Q, Liu H, Zhang B (2014) High-throughput deep sequencing shows that microRNA s play important roles in switchgrass responses to drought and salinity stress. Plant Biotech J 12:354–366. https://doi.org/10.1111/pbi.12142
Yadav A, Sanyal I, Rai SP, Lata C (2021a) An overview on miRNA-encoded peptides in plant biology research. Genomics 113:2385–2391. https://doi.org/10.1016/j.ygeno.2021.05.013
Yadav A, Kumar S, Verma R, Lata C, Sanyal I, Rai SP (2021b) microRNA 166: an evolutionarily conserved stress biomarker in land plants targeting HD-ZIP family. Physiol Mol Biol Plants 27:2471–2485. https://doi.org/10.1007/s12298-021-01096-x
Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4. https://doi.org/10.1016/j.tplants.2008.10.004
Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66:1749–1761. https://doi.org/10.1093/jxb/erv013
Acknowledgements
We pay our thanks to the Director, CSIR-NBRI, Lucknow for his support and guidance. Authors also pay gratitude to Council of Scientific and Industrial Research, New Delhi for funding the research under the project “Genome-wide editing for enhanced yield and quality traits” (MLP0026). AY acknowledges a fellowship from the Department of Science and Technology, Government of India as a senior research fellowship [IF180146]. CSIR-NBRI Manuscript Number NBRI_MS/2021/12/01.
Author information
Authors and Affiliations
Contributions
CL conceived and designed the research. CL and IS provided facilities and funding for the research. AY conducted the experiments and wrote the manuscript. AY, SK and RV analysed the data. CL, SPR and IS critically reviewed the manuscript. All authors read and approved the manuscript. The authors also pay their gratitude to Dr. Puneet Singh Chauhan for providing the Pseudomonas putida bacterial strain (RA).
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Christell van der Vyver.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yadav, A., Kumar, S., Verma, R. et al. Target cleavage mapping and tissue-specific expression analysis of PGPR responsive miR166 under abiotic stress in chickpea (Cicer arietinum L.). Plant Cell Tiss Organ Cult 154, 415–432 (2023). https://doi.org/10.1007/s11240-023-02517-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-023-02517-3