Abstract
Key message
Drought stress response studies and overexpression of vun-miR408 proved it to be essential for abiotic stress tolerance in cowpea.
Abstract
Small RNA and transcriptome sequencing of an elite high-yielding drought-tolerant Indian cowpea cultivar, Pusa Komal revealed a differential expression of 198 highly conserved, 21 legume-specific, 14 less-conserved, and 10 novel drought-responsive microRNAs (miRNAs) along with 3391 (up-regulated) and 3799 (down-regulated) genes, respectively, in the leaf and root libraries. Among the differentially expressed miRNAs, vun-miR408-3p, showed an up-regulation of 3.53-log2-fold change under drought stress. Furthermore, laccase 12 (LAC 12) was identified as the potential target of vun-miR408-3p using 5′ RNA ligase-mediated rapid amplification of cDNA ends. The stable transgenic cowpea lines overexpressing artificial vun-miR408-3p (OX-amiR408) displayed enhanced drought and salinity tolerance as compared to the wild-type plants. An average increase of 30.17% in chlorophyll, 26.57% in proline, and 27.62% in relative water content along with lesser cellular H2O2 level was observed in the transgenic lines in comparison with the wild-type plants under drought stress. Additionally, the scanning electron microscopic study revealed a decrease in the stomatal aperture and an increase in the trichome density in the transgenic lines. The expression levels of laccase 3 and laccase 12, the potential targets of miR408, related to lipid catabolic processes showed a significant reduction in the wild-type plants under drought stress and the transgenic lines, indicating the regulation of lignin content as a plausibly essential trait related to the drought tolerance in cowpea. Taken together, this study primarily focused on identification of drought-responsive miRNAs and genes in cowpea, and functional validation of role of miR408 towards drought stress response in cowpea.
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Data availability
All extracted data from the sequencing of cowpea samples used for this work are available in the Supplementary Data.
References
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30:161–175. https://doi.org/10.3109/07388550903524243
Ahmad P, Tripathi DK, Deshmukh R, Singh VP, Corpas FJ (2019) Revisiting the role of ROS and RNS in plants under changing environment. Environ Exp Bot 161:1–3. https://doi.org/10.1016/j.envexpbot.2019.02.017
Alvarez S, Marsh EL, Schroeder SG, Schachtman DP (2008) Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ 31:325–340. https://doi.org/10.1111/j.1365-3040.2007.01770.x
Arenas-Huertero C, Pérez B, Rabanal F et al (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70:385–401. https://doi.org/10.1007/s11103-009-9480-3
Badhan S, Kole P, Ball A, Mantri N (2018) RNA sequencing of leaf tissues from two contrasting chickpea genotypes reveals mechanisms for drought tolerance. Plant Physiol Biochem 129:295–304. https://doi.org/10.1016/j.plaphy.2018.06.007
Badr A, Brüggmann W (2020) Comparative analysis of drought stress response of maize genotypes using chlorophyll fluorescence measurements and leaf relative water content. Photosynthetica 58: 638–645. https://doi.org/10.32615/ps.2020.014
Barbier FF, Dun EA, Beveridge CA (2017) Apical dominance. Curr Biol 27:R864–R865. https://doi.org/10.1016/j.cub.2017.05.024
Barrera-Figueroa BE, Gao L, Diop NN et al (2011) Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol 11:127. https://doi.org/10.1186/1471-2229-11-127
Begum N, Ahanger MA, Su Y, Lei Y, Mustafa NSA, Ahmad P, Zhang L (2019) Improved Drought Tolerance by AMF Inoculation in Maize (Zea mays) Involves Physiological and Biochemical Implications. Plants 8:579. https://doi.org/10.3390/plants8120579
Ben-Targem M, Ripper D, Bayer M, Ragni L (2021) Auxin and gibberellin signaling cross-talk promotes hypocotyl xylem expansion and cambium homeostasis. J Exp Bot 72:3647–3660. https://doi.org/10.1093/jxb/erab089
Bhat KV, Mondal TK, Gaikwad AB, Kole PR, Chandel G, Mohapatra T (2020) Genome-wide identification of drought-responsive miRNAs in grass pea (Lathyrus sativus L.). Plant Gene 21:100210. https://doi.org/10.1016/j.plgene.2019.100210
Bhattacharya R, Saha S, Kostina O et al (2020) Replacing critical point drying with a low-cost chemical drying provides comparable surface image quality of glandular trichomes from leaves of Millingtonia hortensis L. f. in scanning electron micrograph. Appl Microsc 50:15. https://doi.org/10.1186/s42649-020-00035-6
Brasileiro ACM, Morgante CV, Araujo ACG et al (2015) Transcriptome Profiling of Wild Arachis from Water-Limited Environments Uncovers Drought Tolerance Candidate Genes. Plant Mol Biol Report 33:1876–1892. https://doi.org/10.1007/s11105-015-0882-x
Buch DU, Sharma OA, Pable AA, Barvkar VT (2020) Characterization of microRNA genes from Pigeonpea (Cajanus cajan L.) and understanding their involvement in drought stress. J Biotechnol 321:23–34. https://doi.org/10.1016/j.jbiotec.2020.06.019
Cai H, Yang C, Liu S et al (2019) MiRNA-target pairs regulate adventitious rooting in Populus: a functional role for miR167a and its target Auxin response factor 8. Tree Physiol 39:1922–1936. https://doi.org/10.1093/treephys/tpz085
Carvalho M, Lino-Neto T, Rosa E, Carnide V (2017) Cowpea: a legume crop for a challenging environment. J Sci Food Agric 97:4273–4284. https://doi.org/10.1002/jsfa.8250
Chandra T, Mishra S, Panda BB, Sahu G, Dash SK, Shaw BP (2021) Study of expressions of miRNAs in the spikelets based on their spatial location on panicle in rice cultivars provided insight into their influence on grain development. Plant Physiol Biochem 159:244–256. https://doi.org/10.1016/j.plaphy.2020.12.020
Chu CC, Lee WC, Guo WY, Pan SM, Chen LJ, Li HM, Jinn TL (2005) A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis. Plant Physiol 139:425–436. https://doi.org/10.1104/pp.105.065284
Conde A, Chaves MM, Gerós H (2011) Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol 52:1583–1602. https://doi.org/10.1093/pcp/pcr107
Cravens AE, Henderson J, Friedman J, Burkardt N, Cooper AE, Haigh T, Hayes M, McEvoy J, Paladino S, Wilke AK, Wilmer H (2021) A typology of drought decision making: Synthesizing across cases to understand drought preparedness and response actions. Weather Clim Extrem. https://doi.org/10.1016/j.wace.2021.100362
Dai Y, Sun X, Wang C et al (2021) Gene co-expression network analysis reveals key pathways and hub genes in Chinese cabbage (Brassica rapa L.) during vernalization. BMC Genomics 22:236. https://doi.org/10.1186/s12864-021-07510-8
De Luis A, Markmann K, Cognat V, Holt DB, Charpentier M, Parniske M, Stougaard J, Voinnet O (2012) Two MicroRNAs linked to nodule infection and nitrogen-fixing ability in the legume Lotus japonicus. Plant Physiol 160:2137–2154. https://doi.org/10.1104/pp.112.204883
Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 Transcription Factor Is a Modulator of Phosphate Acquisition and Root Development in Arabidopsis. Plant Physiol 143:1789–1801. https://doi.org/10.1104/pp.106.093971
Farooq A, Bukhari SA, Akram NA, Ashraf M, Wijaya L, Alyemeni MN, Ahmad P (2020) Exogenously Applied Ascorbic Acid-Mediated Changes in Osmoprotection and Oxidative Defense System Enhanced Water Stress Tolerance in Different Cultivars of Safflower (Carthamus tinctorious L.). Plants 9:104. https://doi.org/10.3390/plants9010104
Fasani E, DalCorso G, Zorzi G, Vitulo N, Furini A (2021) Comparative analysis identifies micro-RNA associated with nutrient homeostasis, development and stress response in Arabidopsis thaliana upon high Zn and metal hyperaccumulator Arabidopsis helleri. Physiol Plant. https://doi.org/10.1111/ppl.13488
Feng H, Zhang Q, Wang Q et al (2013) Target of tae-miR408, a chemocyanin-like protein gene (TaCLP1), plays positive roles in wheat response to high-salinity, heavy cupric stress and stripe rust. Plant Mol Biol 83:433–443. https://doi.org/10.1007/s11103-013-0101-9
Goettel W, Liu Z, Xia J, Zhang W, Zhao PX, An YQC (2014) Systems and evolutionary characterization of microRNAs and their underlying regulatory networks in soybean cotyledons. PLoS ONE 9:e86153. https://doi.org/10.1371/journal.pone.0086153
Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: Unraveling the signaling networks. Front Plant Sci 5:151–160. https://doi.org/10.3389/fpls.2014.00151
Guo P, Li Z, Huang P et al (2017) A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid, and reactive oxygen species accelerates leaf senescence. Plant Cell 29:2854–2870. https://doi.org/10.1105/tpc.17.00438
Gupta A, Rico-Medina A, Caño-Delgado AI (2020) The physiology of plant responses to drought. Science 368:266–269. https://doi.org/10.1126/science.aaz7614
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
Hamidou F, Zombre G, Braconnier S (2007) Physiological and biochemical responses of cowpea genotypes to water stress under glasshouse and field conditions. J Agron Crop Sci 193:229–237. https://doi.org/10.1111/j.1439-037X.2007.00253.x
Hang N, Shi T, Liu Y, Ye W, Taier G, Sun Y, Wang K, Zhang W (2021) Overexpression of Os-microRNA408 enhances drought tolerance in perennial ryegrass. Physiol Plant 172:733–747. https://doi.org/10.1111/ppl.13276
Hoffmann N, Benske A, Betz H, Schuetz M, Samuels AL (2020) Laccases and peroxidases co-localize in lignified secondary cell walls throughout stem development. Plant Physiol 184:806–822. https://doi.org/10.1104/pp.20.00473
Hosseini SZ, Ismaili A, Nazarian-Firouzabadi F, Fallahi H, Nejad AR, Sohrabi SS (2021) Dissecting the molecular responses of lentil to individual and combined drought and heat stresses by comparative transcriptomic analysis. Genomics 113:693–705. https://doi.org/10.1016/j.ygeno.2020.12.038
Iuchi S, Yamaguchi-Shinozaki K, Urao T, Terao T, Shinozaki K (1996) Novel drought-inducible genes in the highly drought-tolerant cowpea: cloning of cDNAs and analysis of the expression of the corresponding genes. Plant Cell Physiol 37:1073–1082. https://doi.org/10.1093/oxfordjournals.pcp.a029056
Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2000) A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123:553–562. https://doi.org/10.1104/pp.123.2.553
Jagadeeswaran G, Zheng Y, Li YF, Shukla LI, Matts J, Hoyt P, Macmil SL, Wiley GB, Roe BA, Zhang W, Sunkar R (2009) Cloning and characterization of small RNAs from Medicago truncatula reveals four novel legume-specific microRNA families. New Phytol 184:85–98. https://doi.org/10.1111/j.1469-8137.2009.02915.x
Jha UC, Bohra A, Nayyar H (2020) Advances in “omics” approaches to tackle drought stress in grain legumes. Plant Breed 139:1–27. https://doi.org/10.1111/pbr.12761
Jia X, Wang WX, Ren L et al (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71:51–59. https://doi.org/10.1007/s11103-009-9508-8
Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genomics 10:493–507. https://doi.org/10.1007/s10142-010-0181-4
Kaya C, Ashraf M, Wijaya L, Ahmad P (2019) The putative role of endogenous nitric oxide in brassinosteroid-induced antioxidant defence system in pepper (Capsicum annuum L.) plants under water stress. Plant Physiol Biochem 143:119–128. https://doi.org/10.1016/j.plaphy.2019.08.024
Kaya C, Şenbayram M, Akram NA, Ashraf M, Alyemeni MN, Ahmad P (2020) Sulfur-enriched leonardite and humic acid soil amendments enhance tolerance to drought and phosphorus deficiency stress in maize (Zea mays L.). Sci Rep 10:6432. https://doi.org/10.1038/s41598-020-62669-6
Khodabin G, Tahmasebi-Sarvestani Z, Rad AHS, Modarres-Sanavy SAM (2020) Chem Biodivers 17:e1900399. https://doi.org/10.1002/cbdv.201900399
Kohli SK, Khanna K, Bhardwaj R, Abd Allah EF, Ahmad P, Corpas FJ (2019) Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules. Antioxidants 8:641. https://doi.org/10.3390/antiox8120641
Kosar F, Akram NA, Ashraf M, Ahmad A, Alyemeni MN, Ahmad P (2021) Impact of exogenously applied trehalose on leaf biochemistry, achene yield and oil composition of sunflower under drought stress. Physiol Plant 172:317–333. https://doi.org/10.1111/ppl.13155
Kulcheski FR, De OLFV, Molina LG et al (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307. https://doi.org/10.1186/1471-2164-12-307
Lelandais-Brière C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M (2009) Genome-wide medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21:2780–2796. https://doi.org/10.1105/tpc.109.068130
Leng X, Wang P, Zhao P, Wang M, Cui L, Shangguan L, Wang C (2017) Conservation of microRNA-mediated regulatory networks in response to copper stress in grapevine. Plant Growth Regul 82:293–304. https://doi.org/10.1007/s10725-017-0259-2
Li W, Pang S, Lu Z, Jin B (2020) Function and mechanism of WRKY transcription factors in abiotic stress responses of plants. Plants 9:1515. https://doi.org/10.3390/plants9111515
Liang C, Wang W, Ma J et al (2020) Identification of differentially expressed microRNAs of sunflower seedlings under drought stress. Agron J 112:2472–2484. https://doi.org/10.1002/agj2.20254
Liao H, Wang Q, Zhang N et al (2021) High-throughput microRNA and mRNA sequencing reveals that microRNAs may be involved in peroxidase-mediated cold tolerance in potato. Plant Mol Biol Report. https://doi.org/10.1007/s11105-020-01272-5
Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19:335. https://doi.org/10.3390/ijms19020335
Ma C, Burd S, Lers A (2015) miR408 is involved in abiotic stress responses in Arabidopsis. Plant J 84:169–187. https://doi.org/10.1111/tpj.12999
Ma Q, Xu X, Wang W, Zhao L, Ma D, Xie Y (2021) Comparative analysis of alfalfa (Medicago sativa L.) seedling transcriptomes reveals genotype-specific drought tolerance mechanisms. Plant Physiol Biochem 166:203–214. https://doi.org/10.1016/j.plaphy.2021.05.008
Meißner A, Granzow S, Wemheuer F, Pfeiffer B (2021) The cropping system matters – Contrasting responses of winter faba bean (Vicia faba L.) genotypes to drought stress. J Plant Physiol 263:153463. https://doi.org/10.1016/j.jplph.2021.153463
Mishra S, Behura R, Awasthi JP et al (2014) Ectopic overexpression of a mungbean vacuolar Na+/H+ antiporter gene (VrNHX1) leads to increased salinity stress tolerance in transgenic Vigna unguiculata L. Walp Mol Breed 34:1345–1359. https://doi.org/10.1007/s11032-014-0120-5
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/s1360-1385(02)02312-9
Mutum RD, Balyan SC, Kansal S, Agarwal P, Kumar S, Kumar M, Raghuvanshi S (2013) Evolution of variety-specific regulatory schema for expression of osa-miR408 in indica rice varieties under drought stress. FEBS J 280:1717–1730. https://doi.org/10.1111/febs.12186
Ning P, Wang J, Zhou Y, Gao L, Wang J, Gong C (2016) Adaptional evolution of trichome in Caragana korshinskii to natural drought stress on the Loess Plateau, China. Ecol Evol 6:3786–3795. https://doi.org/10.1002/ece3.2157
Nkomo GV, Sedibe MM, Mofokeng MA (2021) Production constraints and improvement strategies of cowpea (Vigna unguiculata L. Walp.) genotypes for drought tolerance. Int J Agron 2021:1–9. https://doi.org/10.1155/2021/5536417
Nunes-Nesi A, Cavalcanti JHF, Fernie AR (2020) Characterization of in vivo function(s) of members of the plant mitochondrial carrier family. Biomolecules 10:1226. https://doi.org/10.3390/biom10091226
Pagano L, Rossi R, Paesano L, Marmiroli N, Marmiroli M (2021) miRNA regulation and stress adaptation in plants. Environ Exp Bot 184:104369. https://doi.org/10.1016/j.envexpbot.2020.104369
Pokoo R, Ren S, Wang Q et al (2018) Genotype- and tissue-specific miRNA profiles and their targets in three alfalfa (Medicago sativa L) genotypes. BMC Genomics 19:913. https://doi.org/10.1186/s12864-018-5280-y
Ravelombola W, Shi A, Huynh BL (2021) Loci discovery, network-guided approach, and genomic prediction for drought tolerance index in a multi-parent advanced generation intercross (MAGIC) cowpea population. Hortic Res 8:24. https://doi.org/10.1038/s41438-021-00462-w
Rehman AU, Bashir F, Ayaydin F, Kóta Z, Páli T, Vass I (2021) Proline is a quencher of singlet oxygen and superoxide both in in vitro systems and isolated thylakoids. Physiol Plant 172:7–18. https://doi.org/10.1111/ppl.13265
Ren J, Zhang H, Shi X, Ai X, Dong J, Zhao X, Zhong C, Jiang C, Wang J, Yu H (2020) Genome-wide identification of key candidate microRNAs and target genes associated with peanut drought tolerance. DNA Cell Biol 40:373–383. https://doi.org/10.1089/dna.2020.6245
Shigeto J, Nagano M, Fujita K, Tsutsumi Y (2014) Catalytic profile of arabidopsis peroxidases, AtPrx-2, 25 and 71, contributing to stem lignification. PLoS ONE 9:e105332. https://doi.org/10.1371/journal.pone.0105332
Shigeto J, Itoh Y, Hirao S, Ohira K, Fujita K, Tsutsumi Y (2015) Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem. J Integr Plant Biol 57:349–356. https://doi.org/10.1111/jipb.12334
Shui XR, Chen ZW, Li JX (2013) MicroRNA prediction and its function in regulating drought-related genes in cowpea. Plant Sci 210:25–35. https://doi.org/10.1016/j.plantsci.2013.05.002
Song Z, Zhang L, Wang Y, Li H, Li S, Zhao H, Zhang H (2018) Constitutive expression of miR408 improves biomass and seed yield in arabidopsis. Front Plant Sci 8:2114. https://doi.org/10.3389/fpls.2017.02114
Sosa-Valencia G, Palomar M, Covarrubias AA, Reyes JL (2017) The legume miR1514a modulates a NAC transcription factor transcript to trigger phasiRNA formation in response to drought. J Exp Bot 68:2013–2026. https://doi.org/10.1093/jxb/erw380
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 235:46–57. https://doi.org/10.1016/j.plantsci.2015.03.002
Subramanian S, Fu Y, Sunkar R et al (2008) Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 9:160. https://doi.org/10.1186/1471-2164-9-160
Sun L, Zhang A, Zhou Z et al (2015) GLABROUS INFLORESCENCE STEMS3 (GIS3) regulates trichome initiation and development in Arabidopsis. New Phytol 206:220–230. https://doi.org/10.1111/nph.13218
Tamang BG, Li S, Rajasundaram D, Lamichhane S, Fukao T (2021) Overlapping and stress-specific transcriptomic and hormonal responses to flooding and drought in soybean. Plant J. https://doi.org/10.1111/tpj.15276
Trindade I, Capitão C, Dalmay T, Fevereiro MP, Santos DM (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta 231:705–716. https://doi.org/10.1007/s00425-009-1078-0
Turner M, Yu O, Subramanian S (2012) Genome organization and characteristics of soybean microRNAs. BMC Genomics 13:169. https://doi.org/10.1186/1471-2164-13-169
Vakilian KA (2020) Machine learning improves our knowledge about miRNA functions towards plant abiotic stresses. Sci Rep 10:3041. https://doi.org/10.1038/s41598-020-59981-6
Wan L, Li Y, Li S, Li X (2021) Transcriptomic profiling revealed genes involved in response to drought stress in alfalfa. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10287-x
Wang L, Mai Y-X, Zhang Y-C, Luo Q, Yang H-Q (2010) MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL6-IV genes regulate shoot branching in arabidopsis. Mol Plant 3:794–806. https://doi.org/10.1093/mp/ssq042
Wang T, Chen L, Zhao M et al (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:367. https://doi.org/10.1186/1471-2164-12-367
Wang Y, Li L, Tang S et al (2016) Combined small RNA and degradome sequencing to identify miRNAs and their targets in response to drought in foxtail millet. BMC Genet 17:57. https://doi.org/10.1186/s12863-016-0364-7
Wang X, Shen C, Meng P et al (2021) Analysis and review of trichomes in plants. BMC Plant Biol 21:70. https://doi.org/10.1186/s12870-021-02840-x
Wei L, Zhang D, Xiang F, Zhang Z (2009) Differentially expressed miRNAs potentially involved in the regulation of defense mechanism to drought stress in maize seedlings. Int J Plant Sci 170:979–989. https://doi.org/10.1086/605122
Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133:4211–4218. https://doi.org/10.1242/dev.02602
Wu J, Wang L, Wang S (2017) MicroRNAs associated with drought response in the pulse crop common bean (Phaseolus vulgaris L.). Gene 628:78–86. https://doi.org/10.1016/j.gene.2017.07.038
Xie F, Stewart CN Jr, Taki FA, He Q, Liu H, Zhang B (2014) High-throughput deep sequencing shows that microRNAs play important roles in switchgrass responses to drought and salinity stress. Plant Biotechnol J 12:354–366. https://doi.org/10.1111/pbi.12142
Xu X, Wang W, Sun Y, Xing A, Wu Z, Tian Z, Li X, Wang Y (2021) MicroRNA omics analysis of Camellia sinesis pollen tubes in response to low-temperature and Nitric Oxide. Biomolecules 11:930. https://doi.org/10.3390/biom11070930
Yadav AK, Carroll AJ, Estavillo GM, Rebetzke GJ, Pogson BJ (2019) Wheat drought tolerance in the field is predicted by amino acid responses to glasshouse-imposed drought. J Exp Bot 70:4931–4948. https://doi.org/10.1093/jxb/erz224
Yan J, Aznar A, Chalvin C et al (2018) Increased drought tolerance in plants engineered for low lignin and low xylan content. Biotechnol Biofuels 11:195. https://doi.org/10.1186/s13068-018-1196-7
Yasin JK, Mishra BK, Pillai MA et al (2020) Genome wide in-silico miRNA and target network prediction from ṁ Horsegram (Macrotyloma uniflorum) accessions. Sci Rep 10:1–23. https://doi.org/10.1038/s41598-020-73140-x
Zegaoui Z, Planchais S, Cabassa C, Djebbar R, Belbachir OA, Carol P (2017) Variation in relative water content, proline accumulation and stress gene expression in two cowpea landraces under drought. J Plant Physiol 218:26–34. https://doi.org/10.1016/j.jplph.2017.07.009
Zhai J, Jeong DH, de Paoli E et al (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553. https://doi.org/10.1101/gad.177527.111
Zhang H, Zhao X, Li J, Cai H, Wang XD, Li L (2014) MicroRNA408 Is Critical for the HY5-SPL7 Gene Network That Mediates the Coordinated Response to Light and Copper. Plant Cell 26:4933–4953. https://doi.org/10.1105/tpc.114.127340
Zhang Y, Song H, Wang X, Zhou X, Zhang K, Chen X, Liu J, Han J, Wang A (2020) The Roles of Different Types of Trichomes in Tomato Resistance to Cold, Drought, Whiteflies, and Botrytis. Agronomy 10:411. https://doi.org/10.3390/agronomy10030411
Zhao K, Zhang D, Lv K, Zhang X, Cheng Z, Li R, Zhou B, Jiang T (2019) Functional characterization of poplar WRKY75 in salt and osmotic tolerance. Plant Sci 289:110259. https://doi.org/10.1016/j.plantsci.2019.110259
Zheng Y, Jagadeeswaran G, Gowdu K et al (2013) Genome-wide analysis of microRNAs in Sacred Lotus, Nelumbo nucifera (Gaertn). Trop Plant Biol 6:117–130. https://doi.org/10.1007/s12042-013-9127-z
Zhou Y, Liu W, Li X et al (2020) Integration of sRNA, degradome, transcriptome analysis and functional investigation reveals gma-miR398c negatively regulates drought tolerance via GmCSDs and GmCCS in transgenic Arabidopsis and soybean. BMC Plant Biol 20:190. https://doi.org/10.1186/s12870-020-02370-y
Zhu C, Ding Y, Liu H (2011) MiR398 and plant stress responses. Physiol Plant 143:1–9. https://doi.org/10.1111/j.1399-3054.2011.01477.x
Zhu X, Leng X, Sun X, Mu Q, Wang B, Li X, Wang C, Fang J (2015) Discovery of conservation and diversification of miR171 genes by phylogenetic analysis based on global genomes. Plant Genome 8:1–11. https://doi.org/10.3835/plantgenome2014.10.0076
Acknowledgements
SM expresses her sincere gratitude to the funding agency, WISE-KIRAN division, Department of Science and Technology, Government of India for fellowship and financial support for the project (reference number “SR/WOS-A/LS-86/2017”) sanctioned under Women Scientist Scheme-A. SM is also thankful to the project mentor, Birendra Prasad Shaw for supervising the work. SM is grateful to the Director of Institute of Life Sciences (ILS) for the lab facilities. GS is grateful to University Grants Commission (UGC) for fellowship. The authors deeply thank Prof. Arun Jagannath for providing pCAMBIA 2301 plasmid and Dr. María Paula Filippone for EHA105 strain.
Funding
This work was supported under the Women Scientist Scheme-A (WOS-A) by the Department of Science and Technology (DST), Government of India (Project no. SR/WOS-A/LS-86/2017).
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SM and BPS contributed to conceptualizing and designing of the manuscript. SM executed, contributed to the overall data generation and analysis. GS partly managed and executed expression data analysis of transgenic samples. SM wrote the manuscript. SM and BPS jointly revised the manuscript. All authors read and approved the manuscript.
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Communicated by Manzer H. Siddiqui.
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Mishra, S., Sahu, G. & Shaw, B.P. Integrative small RNA and transcriptome analysis provides insight into key role of miR408 towards drought tolerance response in cowpea. Plant Cell Rep 41, 75–94 (2022). https://doi.org/10.1007/s00299-021-02783-5
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DOI: https://doi.org/10.1007/s00299-021-02783-5