Abstract
The miR167 family has been shown to play roles in regulating plant fertility by control the expression of a set of ARF transcription factors. In this study, the precursor of miR167a was cloned from the photo–thermo-sensitive genic male sterile (PTGMS) wheat line BS366. Moreover, we identified the target gene, TaARF8, from PTGMS wheat line BS366, and used the 5′-RACE assay to confirm the cleavage site. Overexpression (OE) of TaemiR167a in Arabidopsis induced male sterility phenotypes, and reduced the expression levels of AtARF6 and AtARF8. Meanwhile, OE of TaemiR167a reduced the content of endogenous jasmonic acid (JA) and indole acetic acid (IAA) in transgenic Arabidopsis lines. In PTGMS wheat line BS366, the expression levels of TaemiR167a were up-regulated in anther tissues during pollen development process, while the transcriptional levels of TaARF8 were down-regulated under sterile conditions. Importantly, TaemiR167a was sensitive to low temperature (10°), and was highly expressed in anther tissues of BS366 at pollen developmental stage 3 in sterile environment. Then, we measured the endogenous JA and IAA in BS366 anther tissues, and found that the accumulation of JA and IAA in anther was abnormal during the pollen development process. These results suggested that TaemiR167a-mediated regulation of TaARF8 and changes of endogenous JA and IAA during pollen developmental process took part in the pollen fertility control in PTGMS wheat line BS366.
Similar content being viewed by others
References
Ambros V (2001) MicroRNAs: tiny regulators with great potential. Cell 107(7):823–826. https://doi.org/10.1016/S0092-8674(01)00616-X
Bai JF, Wang YK, Wang P, Duan WJ, Yuan SH, Sun H, Yuan GL, Ma JX, Wang N, Zhang FT (2017) Uncovering male fertility transition responsive miRNA in a wheat photo-thermosensitive genic male sterile line by deep sequencing and degradome analysis. Front Plant Sci 8:1370. https://doi.org/10.3389/fpls.2017.01370
Boer DR, Freire-Rios A, van den Berg WA, Saaki T, Manfield IW, Kepinski S, López-Vidrieo I, Franco-Zorrilla JM, de Vries SC, Solano R, Weijers D, Coll M (2014) Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 156(3):577–589. https://doi.org/10.1016/j.cell.2013.12.027
Che LX, Tang D, Wang KJ, Wang M, Zhu KM, Yu HX, Gu MH, Cheng ZK (2011) OsAM1 is required for leptotene-zygotene transition in rice. Cell Res 21(4):654–665. https://doi.org/10.1038/cr.2011.7
Du H, Wu N, Fu J, Wang S, Li X, Xiao J, Xiong L (2012) A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J Exp Bot 63(18):6467–6480. https://doi.org/10.1093/jxb/ers300
Fan LM, Wang YF, Wang H, Wu WH (2001) In vitro Arabidopsis pollen germination and characterization of the inward potassium currents in Arabidopsis pollen grain protoplasts. J Exp Bot 52(361):1603–1614. https://doi.org/10.1093/jxb/52.361.1603
Franco-Zorrilla JM, López-Vidriero I, Carrasco JL, Godoy M, Vera P, Solano R (2014) DNA-binding specificities of plant transcription factors and their potential to define target genes. Proc Natl Acad Sci USA 111(6):2367–2372. https://doi.org/10.1073/pnas.1316278111
Gruber AR, Lorenz R, Bernhart SH, Neuböck R, Hofacker IL (2008) The Vienna RNA websuite. Nucleic Acids Res 36:70–74. https://doi.org/10.1093/nar/gkn188
Hong ZL, Delauney AJ, Verma DPS (2001) A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell 13(4):755–768. https://doi.org/10.1105/tpc.13.4.755
Hong LL, Tang D, Zhu KM, Wang KJ, Li M, Cheng ZK (2012) Somatic and reproductive cell development in rice anther is regulated by a putative glutaredoxin. Plant Cell 24(2):577–588. https://doi.org/10.1105/tpc.111.093740
Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17(10):2705–2722. https://doi.org/10.1105/tpc.105.034090
Jung KH, Han MJ, Lee DY, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, Hwang I, An G (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18(11):3015–3032. https://doi.org/10.1105/tpc.106.042044
Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M, Matsuoka M (2004) Loss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development. Plant Cell 16(1):33–44. https://doi.org/10.1105/tpc.017327
Li N, Zhang DS, Liu HS, Yin CS, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006a) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18(11):2999–3014. https://doi.org/10.1105/tpc.106.044107
Li YF, Zhao CP, Zhang FT, Sun H, Sun DF (2006b) Fertility alteration in the photo-thermo-sensitive male sterile line BS20 of wheat (Triticum aestivum L.). Euphytica 151(2):207–213. https://doi.org/10.1007/s10681-006-9141-4
Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao YW, Liang WQ, Zhang DB (2010) Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22(1):173–190. https://doi.org/10.4161/psb.5.9.12562
Li H, Yuan Z, Vizcay-Barrena G, Yang CY, Liang WQ, Zong J, Wilson ZA, Zhang DB (2011) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156(2):615–630. https://doi.org/10.1104/pp.111.175760
Li XY, Gao SQ, Tang YM, Li L, Zhang FJ, Feng BE, Fang ZF, Ma LJ, Zhao CP (2015a) Genome-wide identification and evolutionary analyses of bZIP transcription factors in wheat and its relatives and expression profiles of anther development related TabZIP genes. BMC Genomics 16(1):976. https://doi.org/10.1186/s12864-015-2196-7
Li ZF, Zhang YC, Chen YQ (2015b) MiRNAs and lncRNAs in reproductive development. Plant Sci 238:46–52. https://doi.org/10.1016/j.plantsci.2015.05.017
Lian H, Li X, Liu Z, He Y (2013) HYL1 is required for establishment of stamen architecture with four microsporangia in Arabidopsis. J Exp Bot 64(11):3397–3410. https://doi.org/10.1093/jxb/ert178
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):1–5. https://doi.org/10.1016/j.bbrc.2009.04.028
Liu H, Jia SH, Shen DF, Liu J, Li J, Zhao HP, Han SC, Wang YD (2012) Four AUXIN RESPONSE FACTOR genes downregulated by microRNA167 are associated with growth and development in Oryza sativa. Funct Plant Biol 39(9):736–744. https://doi.org/10.1071/FP12106
Liu N, Wu S, Van Houten J, Wang Y, Ding B, Fei ZJ, Clarke TH, Reed JW, Esther VDK (2014) Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J Exp Bot 65(9):2507–2520. https://doi.org/10.1093/jxb/eru141
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(− Delta Delta C(T)). Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Millar AA, Frank G (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17(3):705–721. https://doi.org/10.1105/tpc.104.027920
Nagpal P (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132(18):4107–4118. https://doi.org/10.1242/dev.01955
Nonomura KI, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15:1728–1740
Nonomura K, Nakano M, Fukuda T, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004a) The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis. Plant Cell 16(4):1008–1020. https://doi.org/10.1105/tpc.020701
Nonomura KI, Nakano M, Murata K, Miyoshi K, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004b) An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis. Mol Genet Genomics 271:121–129. https://doi.org/10.1007/s00438-003-0934-z
Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, Kurata N (2007) A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19(8):2583–2594. https://doi.org/10.1105/tpc.107.053199
Omidvar V, Mohorianu I, Dalmay T, Fellner M (2015) Identification of miRNAs with potential roles in regulation of anther development and male-sterility in 7B-1 male-sterile tomato mutant. BMC Genomics 16:878. https://doi.org/10.1186/s12864-015-2077-0
Ostergaard L, Petersen M, Mattsson O, Mundy J (2002) An Arabidopsis callose synthase. Plant Mol Biol 49(6):559–566. https://doi.org/10.1023/A:1015558231400
Pawlowski WP, Wang CJR, Golubovskaya IN, Szymaniak JM, Shi L, Hamant O, Zhu N, Harper L, Sheridan WF, Cande WZ (2009) Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis. Proc Natl Acad Sci USA 106(9):3603–3608. https://doi.org/10.1073/pnas.0810115106
Reeves PH, Ellis CM, Ploense SE, Wu MF, Yadav V, Tholl D, Chételat A, Haupt I, Kennerley BJ, Hodgens C, Farmer EE, Nagpal P, Reed JW (2012) A regulatory network for coordinated flower maturation. PLoS Genet 8(2):e1002506. https://doi.org/10.1371/journal.pgen.1002506
Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520. https://doi.org/10.1016/s0092-8674(02)00863-2
Ru P, Xu L, Ma H, Huang H (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res 16(5):457–465. https://doi.org/10.1038/sj.cr.7310057
Shen YO, Zhang ZM, Lin HJ, Liu HL, Chen J, Peng H, Cao MJ, Rong TZ, Pan GT (2011) Cytoplasmic male sterility-regulated novel microRNAs from maize. Funct Integr Genomics 11(1):179–191. https://doi.org/10.1007/s10142-010-0202-3
Shi J, Tan HX, Yu XH, Liu YY, Liang WQ, Ranathunge K, Franke RB, Schreiber L, Wang YJ, Kai GY, Shanklin J, Ma H, Zhang DB (2011) Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell 23(6):2225–2246. https://doi.org/10.1105/tpc.111.087528
Smoczynska A, Szweykowska-Kulinska Z (2016) MicroRNA-mediated regulation of flower development in grasses. Acta Biochim Pol 63(4):687–692. https://doi.org/10.18388/abp.2016_1358
Steiner-Lange S, Unte US, Eckstein L, Yang CY, Wilson ZA, Schmelzer E, Dekker K, Saedler H (2010) Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant J 34(4):519–528. https://doi.org/10.1046/j.1365-313X.2003.01745.x
Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97(19):10625–10630. https://doi.org/10.1073/pnas.190264497
Sun YJ, Hord CL, Chen CB, Ma H (2010) Regulation of Arabidopsis early anther development by putative cell–cell signaling molecules and transcriptional regulators. J Integr Plant Biol 49(1):60–68. https://doi.org/10.1111/j.1744-7909.2006.00408.x
Tabata R, Ikezaki M, Fujibe T, Aida M, Tian C, Ueno Y, Yamamoto KT, Machida Y, Nakamura K, Ishiguro S (2010) Arabidopsis auxin response factor6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant Cell Physiol 51(1):164–175. https://doi.org/10.1093/pcp/pcp176
Tang ZH, Zhang LP, Xu CG, Yuan SH, Zhang FT, Zheng YL, Zhao CP (2012) Uncovering small RNA-mediated responses to cold stress in a wheat thermosensitive genic male-sterile line by deep sequencing. Plant Physiol 159(2):721–738. https://doi.org/10.1104/pp.112.196048
Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15(2):533–543. https://doi.org/10.1105/tpc.008417
Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R, Nishizawa NK, Gomi K, Shimada A, Kitano H, Ashikari M, Matsuoka M (2010) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47(3):427–444. https://doi.org/10.1111/j.1365-313x.2006.02795.x
Wan LL, Zha WJ, Cheng XY, Liu C, Lv L, Liu CX, Wang ZQ, Du B, Chen RZ, Zhu LL, He GC (2011) A rice β-1,3-glucanase gene Osg1 is required for callose degradation in pollen development. Planta 233(2):309–323. https://doi.org/10.1007/s00425-010-1301-z
Wang JW, Czech B, Weigel D (2009) MiR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738–749. https://doi.org/10.1016/j.cell.2009.06.014
Wang M, Tang D, Luo Q, Jin Y, Shen Y, Wang KJ, Cheng ZK (2012a) BRK1, a Bub1-related kinase, is essential for generating proper tension between homologous kinetochores at metaphase I of rice meiosis. Plant Cell 24(12):4961–4973. https://doi.org/10.1105/tpc.112.105874
Wang Y, Sun FL, Cao H, Peng HR, Ni ZF, Sun QX, Yao YY (2012b) TamiR159 directed wheat TaGAMYB cleavage and its involvement in anther development and heat response. PLoS ONE 7(11):e48445. https://doi.org/10.1371/journal.pone.0048445
Wang YK, Qiao LY, Bai JF, Wang P, Duan WJ, Yuan SH, Yuan GL, Zhang FT, Zhang LP, Zhao CP (2017) Genome-wide characterization of JASMONATE-ZIM DOMAIN transcription repressors in wheat (Triticum aestivum L.). BMC Genomics 18(1):152. https://doi.org/10.1186/s12864-017-3582-0
Wang YK, Bai JF, Wang P, Duan WJ, Yuan SH, Zhang FT, Gao SQ, Liu LH, Pang BS, Zhang LP, Zhao CP (2018) Comparative transcriptome analysis identifies genes involved in the regulation of the pollen cytoskeleton in a genic male sterile wheat line. Plant Growth Regul 86(1):133–147. https://doi.org/10.1007/s10725-018-0416-2
Wei LQ, Yan LF, Wang T (2011) Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome 12(6):1–16. https://doi.org/10.1186/gb-2011-12-6-r53
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(21):4211–4218. https://doi.org/10.1242/dev.02602
Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4):750–759. https://doi.org/10.1016/j.cell.2009.06.031
Xie KB, Wu CQ, Xiong LZ (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142(1):280–293. https://doi.org/10.2307/20205922
Xing SP, Salinas M, Hhmann S, Berndtgen R, Huijser P (2010) MiR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 22(12):3935–3950. https://doi.org/10.1105/tpc.110.079343
Yang JH, Han SJ, Yoon EK, Lee WS (2006) Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res 34(6):1892–1899. https://doi.org/10.1093/nar/gkl118
Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407(1–2):1–11. https://doi.org/10.1016/j.gene.2007.02.034
Yin ZJ, Shen FF (2010) Identification and characterization of conserved microRNAs and their target genes in wheat (Triticum aestivum). Genet Mol Res 9(2):1186–1196. https://doi.org/10.4238/vol9-2gmr805
Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(2):203–214. https://doi.org/10.1089/10665270050081478
Zhang DS, Liang WQ, Yuan Z, Li N, Shi J, Wang J, Liu YM, Yu WJ, Zhang DB (2008) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant 1(4):599–610. https://doi.org/10.1093/mp/ssn028
Zhang LF, Chia JM, Kumari S, Stein JC, Liu ZJ, Narechania A, Maher CA, Guill K, McMullen MD, Ware D (2009) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5(11):e1000716. https://doi.org/10.1371/journal.pgen.1000716
Zhang H, Liang WQ, Yang XJ, Luo X, Jiang N, Ma H, Zhang DB (2010) Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 22(3):672–689. https://doi.org/10.1105/tpc.109.073668
Zhang YC, Yu Y, Wang CY, Li ZY, Liu Q, Xu J, Liao JY, Wang XJ, Qu LH, Chen F (2013) Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 31(9):848–852. https://doi.org/10.1038/nbt.2646
Zhao XA, de Palma J, Oane R, Gamuyao R, Luo M, Chaudhury A, Hervcb P, Xue Q, Bennett J (2008) OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J 54(3):375–387. https://doi.org/10.1111/j.1365-313X.2008.03426.x
Zhou SR, Wang Y, Li WC, Zhao ZG, Ren YL, Wang Y, Gu SH, Lin QB, Wang D, Jiang L, Su N, Zhang X, Liu LL, Cheng ZJ, Lei CL, Wang JL, Guo XP, Wu FQ, Ikehashi H, Wang HY, Wan JM (2011) Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23(1):111–129. https://doi.org/10.1105/tpc.109.073692
Zhou H, Liu QJ, Li J, Jiang DG, Zhou LY, Wu P, Lu S, Li F, Zhu LY, Liu ZL, Chen LT, Liu YG, Zhuang CX (2012) Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res 22(4):649–660. https://doi.org/10.1038/cr.2012.28
Zhu QH, Ramm K, Shivakkumar R, Dennis ES, Upadhyaya NM (2004) The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice. Plant Physiol 135(3):1514–1525. https://doi.org/10.1104/pp.104.041459
Acknowledgements
We gratefully thank the editor’s efficient works and the good comments and suggestions from two reviewers. This work is supported by National Natural Science Foundation of China (No. 31872881), Beijing Municipal Natural Science Foundation (No. 6182014), BAAFS Science and Technology Innovation Foundation (No. KJCX20180403) and National Key Research Project (No. 2016YFD0101601).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10725_2019_503_MOESM1_ESM.tif
Supplementary material 1 (TIFF 3417 kb) Fig. S1 Analysis of TaemiR167a sequence and structure. a ClustalX nucleic acid sequence alignment between TaemiR167a and the miR167a from Arabidopsis thaliana (At, miRBase accession number MI0000208), Oryza sativa (Os, miRBase accession number MI0000676), Zea mays (Zm, miRBase accession number MI0001475), Sorghum bicolor (Sb, miRBase accession number MI0001513), Glycine max (Gm, miRBase accession number MI0001777). Green values in brackets represented the precursor sequence length of each miR167a and b the secondary structure analysis of six precursor sequences of different miR167a
10725_2019_503_MOESM2_ESM.tif
Supplementary material 2 (TIFF 6223 kb) Fig. S2 Characteristics of TaARF8. a PCR productions of TaARF8-A and -D. M DNA ladder, b the protein sequence alignment of TaARF8-A and TaARF8-D. Red line indicated B3 DNA binding motif, blue line indicated auxin response domain, and green line indicated AUX/IAA domain and c a phylogenetic tree of TaARF8, OsARF8, ZmARF8 and AtARF6 and eight proteins. Os rice, Zm Zea mays, At Arabidopsis
10725_2019_503_MOESM3_ESM.tif
Supplementary material 3 (TIFF 933 kb) Fig. S3 Identification of TaemiR167a cleavage site using the 5’-RACE. a PCR production of 3’-TaARF8 and b the region targeted by TaemiR167a in TaARF8 nucleotide sequence
10725_2019_503_MOESM4_ESM.tif
Supplementary material 4 (TIFF 1963 kb) Fig. S4 The expression patterns of TaemiR167a and its target gene TaARF8 during the stage of pollen developmental process, and the measurement of endogenous JA and IAA. a The expression patterns of TaemiR167a in Jing411 and BS366 anther tissues from pollen developmental stages 1 to 3. Bars indicated means ± SD (n = 3). Black star indicted the significant difference between stages 2 or 3 and 1. *p < 0.05,**p < 0.01, Student’s t-test, b the expression patterns of TaARF8 in Jing411 and BS366 anther tissues from pollen developmental stages 1 to 3. Bars indicated means ± SD (n = 3). Black star indicted the significant difference between stages 2 or 3 and 1. *p < 0.05, **p < 0.01, Student’s t-test, c the content of endogenous JA in Jing411 and BS366 anther tissues from pollen developmental stages 1 to 3. Bars indicated means ± SD (n = 3). Black star indicted the significant difference between stages 2 or 3 and 1. *p < 0.05, Student’s t-test. Black star displayed the significant difference between stages 2 or 3 and 1 and d the concentration of endogenous IAA in Jing411 and BS366 anther tissues from pollen developmental stages 1 to 3. Bars indicated means ± SD (n = 3). Black star indicted the significant difference betweens stage 2 or 3 and 1. *p < 0.05, Student’s t-test. Black star displayed the significant difference between stages 2 or 3 and 1
Rights and permissions
About this article
Cite this article
Wang, Y., Duan, W., Bai, J. et al. Constitutive expression of a wheat microRNA, TaemiR167a, confers male sterility in transgenic Arabidopsis. Plant Growth Regul 88, 227–239 (2019). https://doi.org/10.1007/s10725-019-00503-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-019-00503-4