Abstract
Key message
Wheat miRNA member TaMIR1139 targets genes functional in various families and plays crucial roles in regulating plant Pi starvation tolerance.
Abstract
Through regulating target genes at posttranscriptional or translational level, plant miRNAs are involved in mediating diverse biological processes associated with growth, development, and responses to adverse stresses. In this study, we characterized the expression pattern and function of TaMIR1139, a miRNA member of wheat (T. aestivum) under Pi deprivation. TaMIR1139 precursor is also present in N. tabucum, suggesting the conserved nature of miR1139 across monocots and eudicots. TaMIR1139 targets seven genes within different families. The transcripts abundance of TaMIR1139 was induced upon Pi deprivation and the upregulated expression under Pi starvation was downregulated by the Pi recovery treatment, In contrast, the genes targeted by TaMIR1139 exhibited reduced transcripts upon Pi starvation and their downregulated expression was recovered by Pi-recovery condition, suggesting the regulation of them under TaMIR1139 through a cleavage mechanism. TaMIR1139 overexpression conferred the Pi-deprived plants improved phenotype, biomass, photosynthesis, and Pi acquisition. Transcriptome analysis identified numerous genes involving biological process, cellular components, and molecular function were differentially expressed in the TaMIR1139 overexpression lines, which suggests the TaMIR1139-mediated plant Pi starvation tolerance to be associated with the role of miRNA in extensively modulating the transcript profiling. A phosphate transporter (PT) gene NtPT showed significantly upregulated expression in TaMIR1139 overexpression lines; overexpression of it conferred plants improved Pi acquisition upon Pi starvation, suggesting its contribution to the TaMIR1139-mediated plant low-Pi stress resistance. Our investigation indicates that TaMIR1139 is critical in plant Pi starvation tolerance through transcriptionally regulating the target genes and modulating the Pi stress-defensiveness processes.
Similar content being viewed by others
References
Akpinar BA, Budak H (2016) Dissecting miRNAs in wheat D genome progenitor, Aegilops tauschii. Front Plant Sci 7:606
Akpinar BA, Kantar M, Budak H (2015) Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Funct Integr Genom 15:587–598
Alptekin B, Langridge P, Budak H (2017) Abiotic stress miRNomes in the Triticeae. Funct Integr Genom 17:145–170
Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741
Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011
Bakhshi B, Fard EM, Gharechahi J, Safarzadeh M, Nikpay N, Fotovat R, Azimi MR, Salekdeh GH (2017) The contrasting microRNA content of a drought tolerant and a drought susceptible wheat cultivar. J Plant Physiol 216:35–43
Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999
Beauclair L, Yu A, Bouché N (2010) microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J 62:454–462
Budak H, Khan Z, Kantar M (2014) History and current status of wheat miRNAs using next-generation sequencing and their roles in development and stress. Brief Funct Genom 14(3):189–198
Budak H, Kantar M, Bulut R, Akpinar BA (2015) Stress responsive miRNAs and isomiRs in cereals. Plant Sci 235:1–13
Buiatti M, Christou P, Pastore G (2013) The application of GMOs in agriculture and in food production for a better nutrition: two different scientific points of view. Genes Nutr 8:255–270
Burcu A, Budak H (2017) Wheat miRNA ancestors: evident by transcriptome analysis of A, B, and D genome donors. Funct Integr Genom 17:171–187
Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206
Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421
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
Devaiah BN, Madhuvanthi R, Karthikeyan AS, Raghothama KG (2009) Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant 2:43–58
Ding W, Wang Y, Fang W, Gao S, Li X, Xiao K (2016) TaZAT8, a C2H2-ZFP type transcription factor gene in wheat, plays critical roles in mediating tolerance to Pi deprivation through regulating P acquisition, ROS homeostasis and root system establishment. Physiol Plant 158:297–311
Fasani E, DalCorso G, Varotto C, Li M, Visioli G, Mattarozzi M, Furini A (2017) The MTP1 promoters from Arabidopsis halleri reveal cis-regulating elements for the evolution of metal tolerance. New Phytol 214:1614–1630
Fei X, Yu J, Li Y, Deng X (2017) CrMAPK3 regulates the expression of iron-deficiency-responsive genes in Chlamydomonas reinhardtii. BMC Biochem 18:6
Fu C, Sunkar R, Zhou C, Shen H, Zhang JY, Matts J, Wolf J, Mann DGJ, Stewart JCN, Tang Y, Wang ZY (2012) Overexpression of miR156 in switchgrass (Panicum virgatum L.) results in various morphological alterations and leads to improved biomass production. Plant Biotechnol J 10:443–452
Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043
Gao S, Guo C, Zhang Y, Zhang F, Du X, Gu J, Xiao K (2016) Wheat microRNA member TaMIR444a is nitrogen deprivation-responsive and involves plant adaptation to the nitrogen-starvation stress. Plant Mol Biol Rep 34:931–946
Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698
Gu J, Zhou Z, Li Z, Chen Y, Wang Z, Zhang H, Yang J (2017) Photosynthetic properties and potentials for improvement of photosynthesis in pale green leaf rice under high light conditions. Front Plant Sci 8:1082
Guo C, Li J, Chang W, Zhang L, Cui X, Xiao K (2011) Effects of chromosome substitution on the utilization efficiency of nitrogen, phosphorus, and potassium in wheat. Front Agric China 5:253–261
Guo C, Zhao X, Liu X, Zhang L, Gu J, Li X, Lu W, Xiao K (2013) Function of wheat phosphate transporter gene TaPHT2;1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta 237:1163–1178
Hackenberg M, Shi BJ, Gustafson P, Langridge P (2013) Characterization of phosphorus-regulated miR399 and miR827 and their isomirs in barley under phosphorus-sufficient and phosphorus-deficient conditions. BMC Plant Biol 13:214
Hillwig MS, Lebrasseur ND, Green PJ, Macintosh GC (2008) Impact of transcriptional, ABA-dependent, and ABA-independent pathways on wounding regulation of RNS1 expression. Mol Genet Genom 280:249–261
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195
Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132
Hu B, Wang W, Deng K, Li H, Zhang Z, Zhang L, Chu C (2015) MicroRNA399 is involved in multiple nutrient starvation responses in rice. Front Plant Sci 6:188
Jagadeeswaran G, Zheng Y, Sumathipala N, Jiang H, Arrese EL, Soulages JL et al (2010) Deep sequencing of small RNA libraries reveals dynamic regulation of conserved and novel microRNAs and microRNA-stars during silk worm development. BMC Genom 11:52
Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC et al (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207
Jin Q, Xue Z, Dong C, Wang Y, Chu L, Xu Y (2015) Identification and characterization of microRNAs from tree peony (Paeonia ostii) and their response to copper stress. PLoS One 10:e0117584
Jones-Rhoades M, Bartel D, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53
Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genom 10:493–507
Kantar M, Akpınar BA, Valárik M, Lucas SJ, Doležel J, Hernández P, Budak H (2012) Subgenomic analysis of microRNAs in polyploid wheat. Funct Integr Genom 12:465–479
Karthikeyan AS, Varadarajan DK, Mukatira UT, D’Urzo MP, Damsz B, Raghothama KG (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol 130:221–233
Kaur G, Pati PK (2016) Analysis of cis-acting regulatory elements of respiratory burst oxidase homolog (Rboh) gene families in Arabidopsis and rice provides clues for their diverse functions. Comput Biol Chem 62:104–118
Kumar V, Shriram V, Kavi Kishor PB, Jawali N, Shitole MG (2010) Enhanced proline accumulation and salt stress tolerance of transgenic indica rice by over-expressingP5CSF129A gene. Plant Biotechnol Rep 4:37–48
Kurtoglu KY, Kantar M, Lucas SJ, Budak H (2013) Unique and conserved microRNAs in wheat chromosome 5D revealed by next-generation sequencing. PLoS One 8(7):e69801
Kurtoglu KY, Kantar M, Budak H (2014) New wheat microRNA using whole-genome sequence. Funct Integr Genom 14:363–379
Lei M, Zhu C, Liu Y, Karthikeyan AS, Bressan RA, Raghothama KG, Liu D (2011) Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. New Phytol 189:1084–1095
Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746
Liu J, Cheng X, Liu P, Li D, Chen T, Gu X, Sun J (2017) MicroRNA319-regulated TCPs interact with FBHs and PFT1 to activate CO transcription and control flowering time in Arabidopsis. PLoS Genet 13(5):e1006833
López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123
Lucas SJ, Budak H (2012) Sorting the wheat from the Chaff: identifying miRNAs in genomic survey sequences of Triticum aestivum chromosome 1AL. PLoS One 7(7):e40859
Macková H, Hronková M, Dobrá J et al (2013) Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J Exp Bot 64:2805–2815
Muchhal US, Pardo JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA 93:10519–10523
Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J 31:341–353
Ouyang X, Hong X, Zhao X, Zhang W, He X, Ma W, Teng W, Tong Y (2016) Knockout of the PHOSPHATE 2 gene TaPHO2-A1 improves phosphorus uptake and grain yield under low phosphorus conditions in common wheat. Sci Rep 6:29850
Palatnik JF, Allen E, Wu X, Schommer C, Schwab R et al (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263
Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150:1541–1555
Paul S, Datta SK, Datta K (2015) miRNA regulation of nutrient homeostasis in plants.Front. Plant Sci 6:232
Poirier Y, Bucher M (2002) Phosphate transport and homeostasis in Arabidopsis. Arabidopsis Book 1:e0024
Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693
Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133
Samad AFA, Sajad M, Nazaruddin N, Fauzi IA, Murad AMA, Zainal A, Ismail I (2017) MicroRNA and transcription factor: key players in plant regulatory network. Front Plant Sci 8:565
Schünmann PHD, Richardson AE, Vickers CE, Delhaize E (2004) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol 136:4205–4214
Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642
Sinha SK, Rani M, Bansal N, Gayatri N, Venkatesh K, Mandal PK (2015) Nitrate starvation induced changes in root system architecture, carbon: nitrogen metabolism, and miRNA expression in nitrogen-responsive wheat genotypes. Appl Biochem Biotechnol 177:1299–1312
Slattery RA, VanLoocke A, Bernacchi CJ, Zhu XG (2017) Ort DR 92017) Photosynthesis, light use efficiency, and yield of reduced-chlorophyll soybean mutants in field conditions. Front Plant Sci 8:549
Song C, Yu M, Han J, Wang C, Liu H, Zhang Y, Fang J (2012) Validation and characterization of Citrus sinensis microRNAs and their target genes. BMC Res Notes 5(1):235
Sun Z, Ding C, Li X, Xiao K (2012) Molecular characterization and expression analysis of TaZFP15, a C2H2-type zinc finger transcription factor gene in wheat (Triticum aestivum L.). J Integr Agric 11(1):31–42
Sun F, Guo G, Du J, Guo W, Peng H, Ni Z, Sun Q, Yao Y (2014) Whole-genome discovery of miRNAs and their targets in wheat (Triticum aestivum L.). BMC Plant Biol 14:142
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37(6):914–939
Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687
Wang B, Sun YF, Song N, Wei JP, Wang XJ, Feng H, Yin ZY, Kang ZS (2014a) MicroRNAs involving in cold, wounding and salt stresses in Triticum aestivum L. Plant Physiol Biochem 80:90–96
Wang H, Xu Q, Kong YH, Chen Y, Duan JY, Wu WH, Chen YF (2014b) Arabidopsis WRKY45 transcription factor activates PHOSPHATE TRANSPORTER1;1 expression in response to phosphate starvation. Plant Physiol 164:2020–2029
Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98:10487–10492
Xie K, Shen J, Hou X, Yao J, Li X, Xiao J, Xiong L (2012) Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiol 158:1382–1394
Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. J Integr Plant Biol 50:849–859
Zhao X, Liu X, Guo C, Gu J, Xiao K (2013) Identification and characterization of microRNAs from wheat (Triticum aestivum L.) under phosphorus deprivation. J Plant Biochem Biotechnol 22(1):113–123
Zhao Y, Guo C, Li X, Duan W, Ma C, Guo L, Wen Y, Lu W, Xiao K (2015) Characterization and expression pattern analysis of microRNAs in wheat (Triticum aestivum L.) under drought stress. Biol Plant 59:37–46
Zhao L, Wang C, Zhu F, Li Y (2017) Mild osmotic stress promotes 4-methoxy indolyl-3-methyl glucosinolate biosynthesis mediated by the MKK9–MPK3/MPK6 cascade in Arabidopsis. Plant Cell Rep 36(4):543–555
Zuluaga DL, De Paola D, Janni M, Curci PL, Sonnante G (2017) Durum wheat miRNAs in response tp nitrogen starvation at the grain filling stage. PLoS One 12(8):e0183253
Acknowledgements
This work was supported by the National Natural Science Foundation of China (no. 31371618) and Research Plan of Application Base of Hebei (no. 17962901D).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Eugenio Benvenuto.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liu, Z., Wang, X., Chen, X. et al. TaMIR1139: a wheat miRNA responsive to Pi-starvation, acts a critical mediator in modulating plant tolerance to Pi deprivation. Plant Cell Rep 37, 1293–1309 (2018). https://doi.org/10.1007/s00299-018-2313-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-018-2313-6