Abstract
During their lifespan, sessile plants have to cope with bioavailability of the suboptimal nutrient concentration and have to constantly sense/evolve the connecting web of signal cascades for efficient nutrient uptake, storage, and translocation for proper growth and metabolism. However, environmental fluctuations and escalating anthropogenic activities are making it a formidable challenge for plants. This is adding to (micro)nutrient-deficient crops and nutritional insecurity. Biofortification is emerging as a sustainable and efficacious approach which can be utilized to combat the micronutrient malnutrition. A biofortified crop has an enriched level of desired nutrients developed using conventional breeding, agronomic practices, or advanced biotechnological tools. Nutrient homeostasis gets hampered under nutrient stress, which involves disturbance in short-distance and long-distance cell–cell/cell-organ communications involving multiple cellular and molecular components. Advanced sequencing platforms coupled with bioinformatics pipelines and databases have suggested the potential roles of tiny signaling molecules and post-transcriptional regulators, the microRNAs (miRNAs) in key plant phenomena including nutrient homeostasis. miRNAs are seen as emerging targets for biotechnology-based biofortification programs. Thus, understanding the mechanistic insights and regulatory role of miRNAs could open new windows for exploring them in developing nutrient-efficient biofortified crops. This review discusses significance and roles of miRNAs in plant nutrition and nutrient homeostasis and how they play key roles in plant responses to nutrient imbalances/deficiencies/toxicities covering major nutrients—nitrogen (N), phosphorus (P), sulfur (S), magnesium (Mg), iron (Fe), and zinc (Zn). A perspective view has been given on developing miRNA-engineered biofortified crops with recent success stories. Current challenges and future strategies have also been discussed.
Similar content being viewed by others
Change history
13 June 2022
Handling Editor update.
References
Abiri R, Abdul-Hamid H, Sytar O, Abiri R, Bezerra de Almeida EJr, Sharma SK, Bulgakov VP, Arroo RRJ, Malik S (2021) A brief overview of potential treatments for viral diseases using natural plant compounds: the case of SARS-Cov. Molecules 26:3868. https://doi.org/10.3390/molecules26133868
Adetunji CO et al. (2021) Modified cassava: the last hope that could help to feed the world—recent advances. In: Kavi Kishor, P.B., Rajam, M.V., Pullaiah, T. (eds) Genetically modified crops. Springer, Singapore. https://doi.org/10.1007/978-981-15-5932-7_8
Adhikari S, Ghosh S, Azahar I et al (2018) Sulfate improves cadmium tolerance by limiting cadmium accumulation, modulation of sulfur metabolism and antioxidant defense system in maize. Environ Exp Bot 153:143–162. https://doi.org/10.1016/j.envexpbot.2018.05.008
Alloway BJ (2009) Soil factors associated with zinc deficiency in crops and humans. Environ Geochem Health 31:537–548. https://doi.org/10.1007/s10653-009-9255-4
Arif N, Yadav V, Singh S, Singh S, Ahmad P, Mishra RK, Sharma S, Tripathi DK, Dubey NK, Chauhan DK (2016) Influence of high and low levels of plant-beneficial heavy metal ions on plant growth and development. Front Env Sci 4:1–11. https://doi.org/10.3389/fenvs.2016.00069
Ashworth AJ, Owens PR, Allen FL (2020) Long-term cropping systems management influences soil strength and nutrient cycling. Geoderma 361:114062. https://doi.org/10.1016/j.geoderma.2019.114062
Bai Q, Wang X, Chen X, et al (2018) Wheat miRNA TaemiR408 acts as an essential mediator in plant tolerance to Pi deprivation and salt stress via modulating stress-associated physiological processes. Front Plant Sci 9: https://doi.org/10.3389/fpls.2018.00499
Bao H, Chen H, Chen M et al (2019) Transcriptome-wide identification and characterization of microRNAs responsive to phosphate starvation in Populus tomentosa. Funct Integr Genomics 19:953–972. https://doi.org/10.1007/s10142-019-00692-1
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. https://doi.org/10.1016/S0092-8674(04)00045-5
Bologna NG, Iselin R, Abriata LA et al (2018) Nucleo-cytosolic shuttling of ARGONAUTE1 prompts a revised model of the plant microRNA pathway. Mol Cell 69:709-719.e5. https://doi.org/10.1016/J.MOLCEL.2018.01.007
Borrill P, Connorton JM, Balk J, et al (2014) Biofortification of wheat grain with iron and zinc: integrating novel genomic resources and knowledge from model crops. Front Plant Sci 5. https://doi.org/10.3389/fpls.2014.00053
Broadley MR, White PJ, Hammond JP et al (2007) Zinc in plants. New Phytol 173:677–702. https://doi.org/10.1111/j.1469-8137.2007.01996.x
Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17. https://doi.org/10.1007/s11104-007-9466-3
Campos‐Soriano L, Bundó M, Bach‐Pages M, Chiang SF, Chiou TJ, San Segundo B (2020) Phosphate excess increases susceptibility to pathogen infection in rice. Mol Plant Pathol 21(4):555–570. https://doi.org/10.1111/mpp.12916
Cao A, Jin J, Li S, Wang J (2017) Integrated analysis of mRNA and miRNA expression profiling in rice backcrossed progenies (BC2F12) with different plant height. PloS one. 12(8):e0184106. https://doi.org/10.1371/journal.pone.0184106
Carrió-Seguí À, Ruiz-Rivero O, Villamayor-Belinchón L et al (2019) The altered expression of microrna408 influences the Arabidopsis response to iron deficiency. Front Plant Sci 10:1–13. https://doi.org/10.3389/fpls.2019.00324
Chandra AK, Pandey D, Tiwari A et al (2020) An omics study of iron and zinc homeostasis in finger millet: biofortified foods for micronutrient deficiency in an era of climate change? OMICS: A Journal of Integrative Biology. 24:688–705. https://doi.org/10.1089/omi.2020.0095
Chien P-S, Chiang C-B, Wang Z, Chiou T-J (2017) MicroRNA-mediated signaling and regulation of nutrient transport and utilization. Curr Opin Plant Biol 39:73–79. https://doi.org/10.1016/j.pbi.2017.06.007
Cimini S, Gualtieri C, Macovei A et al (2019) Redox balance-DDR-miRNA triangle: relevance in genome stability and stress responses in plants. Front Plant Sci 10:989. https://doi.org/10.3389/FPLS.2019.00989/BIBTEX
Ding Y, Shi Y, Yang S (2020) Molecular regulation of plant responses to environmental temperatures. Mol Plant 13:544–564. https://doi.org/10.1016/j.molp.2020.02.004
Ding N, Huertas R, Torres-Jerez I et al (2021) Transcriptional, metabolic, physiological and developmental responses of switchgrass to phosphorus limitation. Plant Cell Environ 44:186–202. https://doi.org/10.1111/pce.13872
Dong Z, Han M, National NF-P of the, 2008 undefined (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proceedings of the National Academy of Sciences 105(29):9970–9975. https://doi.org/10.1073/pnas.0803356105
Dos Santos TB, Soares JDM, Lima JE et al (2019) An integrated analysis of mRNA and sRNA transcriptional profiles in Coffea arabica L. roots: insights on nitrogen starvation responses. Funct Integr Genomics 19:151–169. https://doi.org/10.1007/S10142-018-0634-8
Du Q, Wang K, Zou C et al (2018) The PILNCR1 -miR399 regulatory module is important for low phosphate tolerance in maize. Plant Physiol 177:1743–1753. https://doi.org/10.1104/pp.18.00034
Fan K, Wong‐Bajracharya J, Lin X, et al (2021) Differentially expressed microRNAs that target functional genes in mature soybean nodules. Plant Genome 14: https://doi.org/10.1002/tpg2.20103
Foley JK, Michaux KD, Mudyahoto B et al (2021) Scaling up delivery of biofortified staple food crops globally: paths to nourishing millions. Food Nutr Bull 42:116–132. https://doi.org/10.1177/0379572120982501
Fukuda M, Fujiwara T, Nishida S (2020) Roles of non-coding RNAs in response to nitrogen availability in plants. Int J Mol Sci 21:8508 21-8508. https://doi.org/10.3390/IJMS21228508
Garg M, Sharma N, Sharma S, et al (2018) Biofortified crops generated by breeding, agronomy, and transgenic approaches are improving lives of millions of people around the world. Front Nutr 5. https://doi.org/10.3389/fnut.2018.00012
Gemede HF, Ratta N (2014) Antinutritional factors in plant foods: Potential health benefits and adverse effects. Int J Nutr Food Sci 3(4):284–289. https://doi.org/10.11648/j.ijnfs.20140304.18
Ghabooli M, Sadat S, Rooy B et al (2019) miR395 is involved in response to cold stress and modulation of sulfate and phosphate deficiency in Grape (Vitis vinifera). J Plant Mol Breed 7:56–66. https://doi.org/10.22058/JPMB.2020.114871.1193
Grabowska A, Smoczynska A, Bielewicz D et al (2020) Barley microRNAs as metabolic sensors for soil nitrogen availability. Plant Sci 299:110608. https://doi.org/10.1016/j.plantsci.2020.110608
Grewal RK, Saraf S, Deb A, Kundu S (2018) Differentially expressed microRNAs link cellular physiology to phenotypic changes in rice under stress conditions. Plant Cell Physiol 59:2143–2154. https://doi.org/10.1093/PCP/PCY136
Gupta OP, Sharma P, Gupta RK, Sharma I (2014) MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives. Plant Mol Biol 84:1–18. https://doi.org/10.1007/s11103-013-0120-6
Gupta OP, Pandey V, Saini R et al (2020) Identifying transcripts associated with efficient transport and accumulation of Fe and Zn in hexaploid wheat (T. aestivum L.). J Biotechnol 316:46–55. https://doi.org/10.1016/j.jbiotec.2020.03.015
Havlin J, Heiniger R (2020) Soil fertility management for better crop production. Agronomy 10:1349. https://doi.org/10.3390/agronomy10091349
Hawkesford M, Horst W, Kichey T, et al (2012) Functions of macronutrients. In: Marschner’s mineral nutrition of higher plants. Elsevier, pp 135–189. https://doi.org/10.1016/B978-0-12-384905-2.00006-6
He H, He L, Gu M (2014) Role of microRNAs in aluminum stress in plants. Plant Cell Rep 33:831–836. https://doi.org/10.1007/S00299-014-1565-Z
He L, Wang H, Zhao Q et al (2020) Tomato grafting onto Torubamu (Solanum melongena): miR166a and miR395b reduce scion Cd accumulation by regulating sulfur transport. Plant Soil 452:267–279. https://doi.org/10.1007/s11104-020-04564-7
Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551. https://doi.org/10.1007/s00425-002-0920-4
Hossain A, Islam M, Maitra S, Majumder D, Garai S, Mondal M, Ahmed A, Roy A, Skalicky M, Brestic M, Islam T (2021) Neglected and underutilized crop species: are they future smart crops in fighting poverty, hunger and malnutrition under changing climate? In: Neglected and underutilized crops-towards nutritional security and sustainability, pp. 1–50, Springer, Singapore. https://doi.org/10.1007/978-981-16-3876-3_1#DOI
Hsieh LC, Lin SI, Shih ACC, Chen JW, Lin WY, Tseng CY, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151(4):2120–2132. https://doi.org/10.1104/pp.109.147280
Huen A, Bally J, Smith P (2018) Identification and characterisation of microRNAs and their target genes in phosphate-starved Nicotiana benthamiana by small RNA deep sequencing and 5’RACE analysis. BMC Genomics 19:940. https://doi.org/10.1186/s12864-018-5258-9
Jamla M, Patil S, Joshi S et al (2021) MicroRNAs and their exploration for developing heavy metal-tolerant plants. J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10476-2
Jha AB, Warkentin TD (2020) Biofortification of pulse crops: status and future perspectives. Plants 9:73. https://doi.org/10.3390/plants9010073
Jin L-F, Yarra R, Yin X-X et al (2021) Identification and function prediction of iron-deficiency-responsive microRNAs in citrus leaves. 3 Biotech 11:121. https://doi.org/10.1007/s13205-021-02669-z
Kanzana G, Musaza J, Wu F et al (2021) Genome-wide development and application of miRNA-SSR markers in Melilotus genus. Physiol Mol Biol Plants 27:2269–2282. https://doi.org/10.1007/s12298-021-01086-z
Kawashima CG, Yoshimoto N, Maruyama-Nakashita A et al (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321. https://doi.org/10.1111/j.1365-313X.2008.03690.x
Kawashima CG, Matthewman CA, Huang S et al (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66:863–876. https://doi.org/10.1111/j.1365-313X.2011.04547.x
Kehr J (2013) Systemic regulation of mineral homeostasis by micro RNAs. Front Plant Sci 4. https://doi.org/10.3389/fpls.2013.00145
Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137. https://doi.org/10.1016/J.BBAGRM.2011.05.001
Kim S, Yang JY, Xu J et al (2008) Two cap-binding proteins CBP20 and CBP80 are involved in processing primary microRNAs. Plant Cell Physiol 49:1634–1644. https://doi.org/10.1093/PCP/PCN146
Kong WW, Yang ZM (2010) Identification of iron-deficiency responsive microRNA genes and cis-elements in Arabidopsis. Plant Physiol Biochem 48:153–159. https://doi.org/10.1016/j.plaphy.2009.12.008
Köster T, Meyer K, Weinholdt C et al (2014) Regulation of pri-miRNA processing by the hnRNP-like protein AtGRP7 in Arabidopsis. Nucleic Acids Res 42:9925–9936. https://doi.org/10.1093/NAR/GKU716
Kumar V, Khare T, Shriram V, Wani SH (2018) Plant small RNAs: the essential epigenetic regulators of gene expression for salt-stress responses and tolerance. Plant Cell Rep 37:61–75. https://doi.org/10.1007/s00299-017-2210-4
Kurihara Y, National YW-P of the, 2004 undefined (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Natl Acad Sci 34(101):12753–12758. https://doi.org/10.1073/pnas.0403115101
Laubinger S, Sachsenberg T, Zeller G et al (2008) Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Natl Acad Sci 25(105):8795–8800. https://doi.org/10.1073/pnas.0802493105
Li Y, Zhang Y, Shi D et al (2013) Spatial-temporal analysis of zinc homeostasis reveals the response mechanisms to acute zinc deficiency in Sorghum bicolor. New Phytol 200:1102–1115. https://doi.org/10.1111/nph.12434
Li C, Yu X, Bai L et al (2016) Responses of miRNAs and their target genes to nitrogen- or phosphorus-deficiency in grafted cucumber seedlings. Hortic Environ Biotechnol 57:97–112. https://doi.org/10.1007/s13580-016-0092-y
Li L, Yi H, Xue M, Yi M (2017a) miR398 and miR395 are involved in response to SO2 stress in Arabidopsis thaliana. Ecotoxicology 26:1181–1187. https://doi.org/10.1007/s10646-017-1843-y
Li S, Liua K, Zhang S et al (2017b) STV1, a ribosomal protein, binds primary microRNA transcripts to promote their interaction with the processing complex in Arabidopsis. Proc Natl Acad Sci USA 114:1424–1429. https://doi.org/10.1073/pnas.1613069114
Li W, He Z, Zhang L et al (2017c) miRNAs involved in the development and differentiation of fertile and sterile flowers in Viburnum macrocephalum f. keteleeri. BMC Genomics 18:1–17. https://doi.org/10.1186/S12864-017-4180-X/FIGURES/9
Li S, Li M, Liu K et al (2020) MAC5, an RNA-binding protein, protects pri-miRNAs from SERRATE-dependent exoribonuclease activities. Proc Natl Acad Sci USA 117:23982–23990. https://doi.org/10.1073/pnas.2008283117
Liang G, Yu D (2010) Reciprocal regulation among miR395, APS and SULTR2;1 in Arabidopsis thaliana. Plant Signal Behav 5:1257–1259. https://doi.org/10.4161/PSB.5.10.12608
Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS ONE 7:e48951. https://doi.org/10.1371/journal.pone.0048951
Liang G, Ai Q, Yu D (2015) Uncovering miRNAs involved in crosstalk between nutrient deficiencies in Arabidopsis. Sci Rep 5:11813. https://doi.org/10.1038/srep11813
Liang WW, Huang JH, Li CP et al (2017) MicroRNA-mediated responses to long-term magnesium-deficiency in Citrus sinensis roots revealed by Illumina sequencing. BMC Genomics 18:1–16. https://doi.org/10.1186/s12864-017-3999-5
Liu M, Tan X, Yang Y et al (2020a) Analysis of the genetic architecture of maize kernel size traits by combined linkage and association mapping. Plant Biotechnol J 18:207–221. https://doi.org/10.1111/pbi.13188
Liu X, Chu S, Sun C et al (2020b) Genome-wide identification of low phosphorus responsive microRNAs in two soybean genotypes by high-throughput sequencing. Funct Integr Genomics 20:825–838. https://doi.org/10.1007/s10142-020-00754-9
López-Ruiz BA, Juárez-González VT et al (2019) Development-related miRNA expression and target regulation during staggered in vitro plant regeneration of Tuxpeño VS-535 Maize Cultivar. Int J Mol Sci 20:2079. https://doi.org/10.3390/IJMS20092079
MacFarlane L-A, Murphy PR (2010) MicroRNA: biogenesis, function and role in cancer. Curr Genomics 11:537–561. https://doi.org/10.2174/138920210793175895
Mahler RL (2004) Nutrients plants require for growth. CIS1124 Publishing University of Idaho College of Agricultural and Life Sciences. http://www.cals.uidaho.edu/edcomm/pdf/CIS/CIS1124.pdf. Accessed 21 Dec 2021
Marques E, Darby HM, Kraft J (2021) Benefits and limitations of non-transgenic micronutrient biofortification approaches. Agronomy 11(3):464. https://doi.org/10.3390/agronomy11030464
Moharil MP, Ingle KP, Jadhav PV, Gawai DC, Khelurkar VC, Suprasanna P (2019) Foxtail millet (Setaria italica L.): potential of smaller millet for future breeding. In: Advances in plant breeding strategies: cereals pp. 133–163). Springer, Cham. https://doi.org/10.1007/978-3-030-23108-8_4
Mosa KA, Ali MA, Ramamoorthy K, Ismail A (2022) Exploring the relationship between plant secondary metabolites and macronutrient homeostasis. In: Kumar V, Srivastava AK, Suprasanna P (Eds) Plant nutrition and food security in the era of climate change, Academic Press, pp119–146. https://doi.org/10.1016/B978-0-12-822916-3.00007-X
O Brien J, Hayder H, Zayed Y, Peng C (2018) Overview of microrna biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne) 9. https://doi.org/10.3389/FENDO.2018.00402/FULL
Ohkama-Ohtsu N, Wasaki J (2010) Recent progress in plant nutrition research: cross-talk between nutrients, plant physiology and soil microorganisms. Plant Cell Physiol 51:1255–1264. https://doi.org/10.1093/pcp/pcq095
Otun S, Escrich A, Achilonu I, Rauwane M, Alexis J, Lerma-Escalera, Morones-Ramírez JR, Rios-Solis L. (2022) The future of cassava in the era of biotechnology in Southern Africa. Crit Rev Biotechnol. https://doi.org/10.1080/07388551.2022.2048791
Paul S, Gayen D, Datta SK, Datta K (2016) Analysis of high iron rice lines reveals new miRNAs that target iron transporters in roots. J Exp Bot 67:5811–5824. https://doi.org/10.1093/jxb/erw346
Paul S, Datta SK, Datta K (2015) miRNA regulation of nutrient homeostasis in plants. Front Plant Sci 06. https://doi.org/10.3389/fpls.2015.00232
Qiao Q, Wang X, Yang M et al (2018) Wheat miRNA member TaMIR2275 involves plant nitrogen starvation adaptation via enhancement of the N acquisition-associated process. Acta Physiol Plant 40:183. https://doi.org/10.1007/s11738-018-2758-9
Reinhart BJ, Weinstein EG, Rhoades MW et al (2002) MicroRNAs in plants. Genes Dev 16:1616–1626. https://doi.org/10.1101/GAD.1004402
Ritchie H, Reay DS, Higgins P (2018) Quantifying, projecting, and addressing India’s hidden hunger. Front Sustain Food Syst 2. https://doi.org/10.3389/fsufs.2018.00011
Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–2399. https://doi.org/10.1105/TPC.113.113159
Sagwal V, Sihag P, Singh Y et al (2022) Development and characterization of nitrogen and phosphorus use efficiency responsive genic and miRNA derived SSR markers in wheat. Heredity 7:1. https://doi.org/10.1038/s41437-022-00506-4
Saltzman A, Birol E, Oparinde A et al (2017) Availability, production, and consumption of crops biofortified by plant breeding: current evidence and future potential. Ann N Y Acad Sci 1390:104–114. https://doi.org/10.1111/nyas.13314
Sega P, Kruszka K, Bielewicz D et al (2021) Pi-starvation induced transcriptional changes in barley revealed by a comprehensive RNA-Seq and degradome analyses. BMC Genomics 22:1–25. https://doi.org/10.1186/s12864-021-07481-w
Shahzad R, Harlina PW, Ayaad M et al (2018) Dynamic roles of microRNAs in nutrient acquisition and plant adaptation under nutrient stress: a review. Plant Omics 11:58–79. https://doi.org/10.21475/poj.11.01.18.pne1014
Shi W, Liu W, Ma C et al (2020) Dissecting microRNA–mRNA regulatory networks underlying sulfur assimilation and cadmium accumulation in poplar leaves. Plant Cell Physiol 61:1614–1630. https://doi.org/10.1093/pcp/pcaa084
Shin S-Y, Jeong JS, Lim JY et al (2018) Transcriptomic analyses of rice (Oryza sativa) genes and non-coding RNAs under nitrogen starvation using multiple omics technologies. BMC Genomics 19:532. https://doi.org/10.1186/s12864-018-4897-1
Shoeb E, Hefferon K (2022) Crop biofortification and food security, In: Kumar V, Srivastava AK, Suprasanna P (Eds) Plant nutrition and food security in the era of climate change, Academic Press, 423–436. https://doi.org/10.1016/B978-0-12-822916-3.00018-4
Shriram V, Kumar V, Devarumath RM, et al (2016) MicroRNAs as potential targets for abiotic stress tolerance in plants. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.00817
Speth C, Willing E-M, Rausch S et al (2013) RACK 1 scaffold proteins influence mi RNA abundance in Arabidopsis. Wiley Online Libr 76:433–445. https://doi.org/10.1111/tpj.12308
Srivastava S, Suprasanna P (2021) MicroRNAs: tiny, powerful players of metal stress responses in plants. Plant Physiol Biochem 166:928–938. https://doi.org/10.1016/j.plaphy.2021.07.004
Sytar O, Cai Z, Brestic M, Kumar A, Prasad MNV, Taran N, Smetanska I (2013) Foliar applied nickel on buckwheat (Fagopyrum esculentum) induced phenolic compounds as potential antioxidants. Clean: Soil, Air, Water 41:1129–1137. https://doi.org/10.1002/clen.201200512
Sytar O, Brestic M, Hajihashemi S, Skalicky M, Kubeš J, Lamilla-Tamayo L, Ibrahimova U, Ibadullayeva S, Landi M (2021) COVID-19 prophylaxis efforts based on natural antiviral plant extracts and their compounds. Molecules 26:727. https://doi.org/10.3390/molecules26030727
Vinoth A, Ravindhran R (2017) Biofortification in millets: a sustainable approach for nutritional security. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00029
Virk PS, Andersson MS, Arcos J, et al (2021) Transition from targeted breeding to mainstreaming of biofortification traits in crop improvement programs. Front Plant Sci 12. https://doi.org/10.3389/fpls.2021.703990
Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687. https://doi.org/10.1016/J.CELL.2009.01.046
Wang L, Song X, Gu L et al (2013) NOT2 proteins promote polymerase II–dependent transcription and interact with multiple microRNA biogenesis factors in Arabidopsis. Plant Cell 25:715–727. https://doi.org/10.1105/TPC.112.105882
Wang Y, Zhang J, Cui W et al (2017) Improvement in fruit quality by overexpressing miR399a in woodland strawberry. J Agric Food Chem 65:7361–7370. https://doi.org/10.1021/acs.jafc.7b01687
Wang Z, Ma Z, Castillo-González C et al (2018) SWI2/SNF2 ATPase CHR2 remodels pri-miRNAs via Serrate to impede miRNA production. Nature 557:516–521. https://doi.org/10.1038/s41586-018-0135-x
Wang S, Sun S, Guo R, et al (2021) Transcriptomic profiling of fe-responsive lncrnas and their regulatory mechanism in rice. Genes (Basel) 12. https://doi.org/10.3390/genes12040567
Wani SH, Kumar V, Khare T et al (2020) miRNA applications for engineering abiotic stress tolerance in plants. Biologia (bratisl) 75:1063–1081. https://doi.org/10.2478/S11756-019-00397-7
Wu X, Shi Y, Li J et al (2013) A role for the RNA-binding protein MOS2 in microRNA maturation in Arabidopsis. Cell Res 23:645–657. https://doi.org/10.1038/cr.2013.23
Xu J, Hou QM, Khare T et al (2019) Exploring miRNAs for developing climate-resilient crops: a perspective review. Sci Total Environ 653:91–104. https://doi.org/10.1016/J.SCITOTENV.2018.10.340
Yang Z, Wang Z, Yang C et al (2019) Physiological responses and small RNAs changes in maize under nitrogen deficiency and resupply. Genes Genomics 41:1183–1194. https://doi.org/10.1007/s13258-019-00848-0
Yang S, Zhang Z, Chen W et al (2021) Integration of mRNA and miRNA profiling reveals the heterosis of three hybrid combinations of Capsicum annuum varieties. GM Crops Food 12:224–241. https://doi.org/10.1080/21645698.2020.1852064
Yu C, Chen Y, Cao Y et al (2018) Overexpression of miR169o, an overlapping microRNA in response to both nitrogen limitation and bacterial infection, promotes nitrogen use efficiency and susceptibility to bacterial blight in rice. Plant Cell Physiol 59:1234–1247. https://doi.org/10.1093/pcp/pcy060
Yuan N, Yuan S, Li Z et al (2016) Heterologous expression of a rice miR395 gene in Nicotiana tabacum impairs sulfate homeostasis. Sci Rep 6:1–14. https://doi.org/10.1038/srep28791
Zeng H, Wang G, Hu X et al (2014) Role of microRNAs in plant responses to nutrient stress. Plant Soil 374:1005–1021. https://doi.org/10.1007/s11104-013-1907-6
Zeng H, Zhang X, Ding M, Zhu Y (2019) Integrated analyses of miRNAome and transcriptome reveal zinc deficiency responses in rice seedlings. BMC Plant Biol 19:585. https://doi.org/10.1186/s12870-019-2203-2
Zhan J, Chu Y, Wang Y et al (2021) The miR164-GhCUC2-GhBRC1 module regulates plant architecture through abscisic acid in cotton. Plant Biotechnol J 19:1839–1851. https://doi.org/10.1111/pbi.13599
Zhang S, Xie M, Ren G, Yu B (2013) CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts. Proc Natl Acad Sci USA 110:17588–17593. https://doi.org/10.1073/pnas.1310644110
Zhang S, Liu Y, Yu B (2014) PRL1, an RNA-binding protein, positively regulates the accumulation of miRNAs and siRNAs in Arabidopsis. PLOS Genet 10:e1004841. https://doi.org/10.1371/JOURNAL.PGEN.1004841
Zhang S, Dou Y, Li S et al (2018) DAWDLE interacts with DICER-like proteins to mediate small RNA biogenesis. Plant Physiol 177:1142–1151. https://doi.org/10.1104/PP.18.00354
Zhang B, You C, Zhang Y et al (2020) Linking key steps of microRNA biogenesis by TREX-2 and the nuclear pore complex in Arabidopsis. Nat Plants 6:957. https://doi.org/10.1038/S41477-020-0726-Z
Zhou J, Wu JT (2022) Nitrate/ammonium-responsive microRNA-mRNA regulatory networks affect root system architecture in Populus× canescens. BMC Plant Biol 22:1–5. https://doi.org/10.1186/s12870-022-03482-3
Zhu FR, Qiu ZB, Zhang YM et al (2020) Characterization and functional analysis of microRNA399 in Cunninghamia lanceolata. Biol Plant 64:193–199. https://doi.org/10.32615/bp.2020.037
Zuluaga DL, De Paola D, Janni M et al (2017) Durum wheat miRNAs in response to nitrogen starvation at the grain filling stage. PLoS ONE 12:e0183253. https://doi.org/10.1371/journal.pone.0183253
Acknowledgements
VK acknowledge the DST-FIST Program (SR/FST/COLLEGE-/19/568), DBT-Star College (BT/HRD/11/030/2012), and DBT-BUILDER (BT/INF/22/SP45363/2022) programs implemented at the Modern College, Ganeshkhind, Pune, India.
Author information
Authors and Affiliations
Contributions
VK and BNT conceived the idea, wrote, and revised the manuscript. All the authors collected the literature, discussed, wrote, and revised the manuscript. All the authors have approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Handling Editor: Peter Nick
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Jamla, M., Joshi, S., Patil, S. et al. MicroRNAs modulating nutrient homeostasis: a sustainable approach for developing biofortified crops. Protoplasma 260, 5–19 (2023). https://doi.org/10.1007/s00709-022-01775-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-022-01775-w