Transcriptome-wide identification and expression profiling of Pinus massoniana MYB transcription factors responding to phosphorus deficiency

Fuhua Fan , Qingzhu Wang , Xiaopeng Wen , Guijie Ding

Journal of Forestry Research ›› 2019, Vol. 31 ›› Issue (3) : 909 -919.

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Journal of Forestry Research ›› 2019, Vol. 31 ›› Issue (3) : 909 -919. DOI: 10.1007/s11676-019-00911-2
Original Paper

Transcriptome-wide identification and expression profiling of Pinus massoniana MYB transcription factors responding to phosphorus deficiency

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Abstract

Myeloblastosis (MYB) proteins constitute one of the largest transcription factor (TF) families in plants and play crucial roles in regulating plant physiological and biochemical processes, including adaptation to diverse abiotic stresses. These TF families contain highly conserved MYB repeats (1R, R2R3, 3R and 4R) at the N-terminus. Roles for MYB TFs have been reported in response to such stresses as dehydration, salt, cold, and drought. The characterization of Masson pine (Pinus massoniana) MYB TFs are reported, including the analysis of MYB TFs expression in seedlings under controlled conditions and two different phosphate (Pi) deficient treatments. By searching for conserved MYB motifs in full transcriptomic RNA sequencing data for P. massoniana, 59 sequences were identified as MYB TFs. Conserved domain structures and comparative functional and phylogenetic relationships of these MYB TFs with those in Arabidopsis were assessed using various bioinformatics tools. Based on microarray analysis, P. massoniana MYB genes exhibited different expression patterns under the two Pi deficiency conditions. Genes encoding MYB TFs that showed increased expression under critical Pi deficiency were identified, and some MYBs were differentially expressed only under conditions of severe Pi starvation. These results are useful for the functional characterization of MYB TFs that may be involved in the response to Pi deficiency and play divergent roles in plants.

Keywords

MYB transcription factors / Transcriptome / Pinus massoniana / Phosphorus deficiency / Microarray analysis

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Fuhua Fan, Qingzhu Wang, Xiaopeng Wen, Guijie Ding. Transcriptome-wide identification and expression profiling of Pinus massoniana MYB transcription factors responding to phosphorus deficiency. Journal of Forestry Research, 2019, 31(3): 909-919 DOI:10.1007/s11676-019-00911-2

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References

[1]

Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell, 2003, 15: 63-78.

[2]

Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem, 2006, 281: 37636-37645.

[3]

Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res, 1997, 25: 3389-3402.

[4]

Baek D, Kim MC, Chun HJ, Kang S, Park HC, Shin G, Park J, Shen M, Hong H, Kim WY, Kim DH, Lee SY, Bressan RA, Bohnert HJ, Yun DJ. Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol, 2013, 161(1): 362-373.

[5]

Cai H, Tian S, Dong H. Large scale in silico identification of MYB family genes from wheat expressed sequence tags. Mol Biotechnol, 2012, 52(2): 184-192.

[6]

Dai X, Wang Y, Yang A, Zhang WH. OsMYB2P-1, and R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiol, 2012, 159: 169-183.

[7]

Denekamp M, Smeekens SC. Integration of wounding and osmotic stress signals determines the expression of the AtMYB102 transcription factor gene. Plant Physiol, 2003, 132: 1415-1423.

[8]

Devaiah BN, Madhuvanthi R, Athikkattuvalasu R, Karthikeyan S, Raghothama KG. Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant, 2009, 2: 43-58.

[9]

Ding Z, Li S, An X, Liu X, Qin H, Wang D. Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Genet Genomics, 2009, 36: 17-29.

[10]

Du H, Yang SS, Liang Z, Feng BR, Liu L, Huang YB, Tang YX. Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biol, 2012, 12: 106.

[11]

Dubos C, Le Gourrierec J, Baudry A, Huep G, Lanet E, Debeaujon I, Lepiniec L. MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J, 2008, 55(6): 940-953.

[12]

Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant Sci, 2010, 15(10): 573-581.

[13]

Fan F, Cui B, Zhang T, Qiao G, Ding G, Wen X. The temporal transcriptomic response of Pinus massoniana seedlings to phosphorus deficiency. PLoS ONE, 2014 9 8 e105068

[14]

Feng S, Xu Y, Yang L, Sun S, Wang D, Chen X. Genome-wide identification and characterization of R2R3-MYB transcription factors in pear. Sci Hortic, 2015, 197: 176-182.

[15]

Ganesan G, Sankararamasubramanian HM, Harikrishnan M, Ganpudi A, Parida A. A MYB transcription factor from the grey mangrove is induced by stress and confers NaCl tolerance in tobacco. J Exp Bot, 2012, 63: 4549-4561.

[16]

Ito M. Conservation and diversification of three-repeat Myb transcription factors in plants. J Plant Res, 2005, 118: 61-69.

[17]

Jin H, Martin C. Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol, 1999, 41: 577-585.

[18]

Jin JP, Tian F, Yang DC, Meng YQ, Kong L, Luo JC, Gao G. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res, 2017, D45(11): D1040-D1045.

[19]

Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V, Bansal KC. Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genom, 2012 13 1 544

[20]

Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS. KANADI regulates organ polarity in Arabidopsis. Nature, 2001, 411(6838): 706-709.

[21]

Kim JH, Nguyen NH, Jeong CY, Nguyen NT, Hong SW, Lee H. Loss of the R2R3 MYB, AtMyb73, causes hyper-induction of the SOS1 and SOS3 genes in response to high salinity in Arabidopsis. J Plant Physiol, 2013, 170(6): 1461-1465.

[22]

Klempnauer K, Gonda T, Bishop J. Nucleotide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: the architecture of a transduced oncogene. Cell, 1982, 31: 453-463.

[23]

Kobayashi K, Suzuki T, Iwata E, Nakamichi N, Suzuki T, Chen P, Ohtani M, Ishida T, Hosoya H, Müller S, Leviczky T, Pettkó-Szandtner A, Darula Z, Iwamoto A, Nomoto M, Tada Y, Higashiyama T, Demura T, Doonan JH, Hauser MT, Sugimoto K, Umeda M, Magyar Z, Bögre L, Ito M. Transcription repression by MYB3R proteins regulates plant organ growth. EMBO J, 2015, 34: 1992-2007.

[24]

Letunic I, Doerks T, Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res, 2012, 40(1): 302-305.

[25]

Liao W, Yang Y, Li Y, Wang G, Peng M. Genome-wide identification of cassava R2R3 MYB family genes related to abscission zone separation after environmental stress-induced abscission. Sci Rep, 2016, 6: 32006.

[26]

Lotkowska ME, Tohge T, Fernie AR, Xue GP, Balazadeh S, Mueller-Roeber B. The Arabidopsis transcription factor MYB112 promotes anthocyanin formation during salinity and under high light stress. Plant Physiol, 2015, 169: 1862-1880.

[27]

Matus JT, Aquea F, Arce-Johnson P. Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol, 2008, 8: 83.

[28]

Mehra P, Pandey BK, Giri J. Improvement in phosphate acquisition and utilization by a secretory purple acid phosphatase (OsPAP21b) in rice. Plant Biotechnol J, 2017

[29]

Muthamilarasan M, Bonthala VS, Khandelwal R, Jaishankar J, Shweta S, Nawaz K, Prasad M. Global analysis of WRKY transcription factor superfamily in Setaria identifies potential candidates involved in abiotic stress signaling. Front Plant Sci, 2015, 6: 910.

[30]

Ogata K, Hojo H, Aimoto S, Nakai T, Nakamura H, Sarai A, Ishii S, Nishimura Y. Solution structure of a DNA-binding unit of MYB: a helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core. Proc Natl Acad Sci USA, 1992, 89: 6428-6432.

[31]

Pandey BK, Mehra P, Verma L, Bhadouria J, Giri J. OsHAD1, a haloacid dehalogenase-like APase enhances phosphate accumulation. Plant Physiol, 2017

[32]

Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H. The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J, 1987, 6: 3553-3558.

[33]

Peng X, Liu H, Wang D, Shen S. Genome-wide identification of the Jatrophacurcas MYB family and functional analysis of the abiotic stress responsive gene JcMYB2. BMC Genom, 2016, 17: 251.

[34]

Ren F, Guo QQ, Chang LL, Chen L, Zhao CZ, Zhong H, Li XB. Brassica napus PHR1 gene encoding a MYB-like protein functions in response to phosphate starvation. PLoS ONE, 2012 7 8 e44005

[35]

Rose A, Meier I, Wienand U. The tomato I-box binding factor LeMYBI is a member of a novel class of MYB-like proteins. Plant J, 1999, 20: 641-652.

[36]

Rosinski JA, Atchley WR. Molecular evolution of the Myb family of transcription factors: evidence for polyphyletic origin. J Mol Evol, 1998, 46: 74-83.

[37]

Ruan W, Guo M, Wu P, Yi K. Phosphate starvation induced OsPHR4 mediates Pi-signaling and homeostasis in rice. Plant Mol Biol, 2017, 93(3): 327-340.

[38]

Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev, 2001, 15(6): 2122-2133.

[39]

Seo PJ, Park CM. Auxin homeostasis during lateral root development under drought condition. Plant Signal Behav, 2009, 4: 1002-1004.

[40]

Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM. The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell, 2011, 23: 1138-1152.

[41]

Shen J, Yan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F. Phosphorus dynamics: from soil to plant. Plant Physiol, 2011, 156(3): 997-1005.

[42]

Simon M, Lee MM, Lin Y, Gish L, Schiefelbein J. Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Dev Biol, 2007, 311(2): 566-578.

[43]

Stracke R, Holtgräwe D, Schneider J, Pucker B, Sörensen TR, Weisshaar B. Genome-wide identification and characterization of R2R3-MYB genes in sugar beet (Beta vulgaris). BMC Plant Biol, 2014 14 1 249

[44]

Su L, Wang Y, Liu D, Li X, Zhai Y, Sun X, Li X, Liu Y, Li J, Wang Q. The soybean gene, GmMYNJ2, encodes a R2R3-type transcription factor involved in drought stress tolerance in Arabidopsis thaliana. Acta Physiol Plant, 2015, 37: 138.

[45]

Tombuloglu H, Kekec G, Sakcali MS, Unver T. Transcriptome-wide identification of R2R3-MYB transcription factors in barley with their boron responsive expression analysis. Mol Genet Genomics, 2013, 288: 141-155.

[46]

Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K. An Arabidopsis myb homologs is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell, 1993, 5: 1529-1539.

[47]

Wang J, Sun J, Miao J, Guo J, Shi Z, He M, Chen Y, Zhao X, Li B, Han F, Tong Y, Li Z. A phosphate starvation response regulator Ta-PHR1 is involved in phosphate signaling and increases grain yield in wheat. Ann Bot, 2013, 111: 1139-1153.

[48]

Wang F, Suo Y, Wei H, Li M, Xie C, Wang L, Chen X, Zhang Z. Identification and characterization of 40 isolated Rehmannia glutinosa MYB family genes and their expression profiles in response to shading and continuous cropping. Int J Mol Sci, 2015, 16: 15009-15030.

[49]

Waters MT, Wang P, Korkaric M, Capper RG, Saunders NJ, Langdale JA. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell, 2009, 21(4): 1109-1128.

[50]

Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM. Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol, 2009, 149(2): 981-993.

[51]

Yang A, Dai XY, Zhang WH. A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bor, 2012, 63: 2541-2556.

[52]

Zhang Y, Zhou Z, Ma X, Jin G. Foraging ability and growth performance of four subtropical tree species in response to heterogeneous nutrient environments. J For Res, 2010, 15: 91-98.

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