Analysis of differential expression of genes induced by ethephon in elongating internodes of maize plants

Xiaoyi WEI, Weiqiang ZHANG, Qian ZHANG, Pei SUN, Zhaohu LI, Mingcai ZHANG, Jianmin LI, Liusheng DUAN

PDF(1283 KB)
PDF(1283 KB)
Front. Agr. Sci. Eng. ›› 2016, Vol. 3 ›› Issue (3) : 263-282. DOI: 10.15302/J-FASE-2016103
RESEARCH ARTICLE
RESEARCH ARTICLE

Analysis of differential expression of genes induced by ethephon in elongating internodes of maize plants

Author information +
History +

Abstract

Plant growth regulators (PGRs) are commonly used in cereal cropping systems to restrict plant height and control lodging. Ethephon has been reported to shorten internodes and increase grain yield of maize. To analyze the transcriptomic profiles of maize internode elongation following ethephon treatment, differentially expressed genes were compared between the treatment and control samples of inbred line Zong 31 using the Affymetrix Maize Genome Array. According to the microarray data, 326 probe sets showed significant change in expression. Further research revealed that the most remarkable effects of ethephon on maize internodes elongation occurred during a 48 h period, when 89 differentially expressed genes were detected. There were dramatic change in transcript levels at 24 h and six Auxin transport genes and four gibberellin biosynthesis pathway genes were differentially expressed in Zong 31 in response to ethephon treatment. In summary, we showed that gaseous ethylene release is involved in internode meristem cell elongation through the regulation of plant hormone signaling in maize. This work provides a platform for studies in which candidate genes will be functionally tested for involvement in internode elongation.

Keywords

maize / ethephon / internode elongation / microarray / qPCR

Cite this article

Download citation ▾
Xiaoyi WEI, Weiqiang ZHANG, Qian ZHANG, Pei SUN, Zhaohu LI, Mingcai ZHANG, Jianmin LI, Liusheng DUAN. Analysis of differential expression of genes induced by ethephon in elongating internodes of maize plants. Front. Agr. Sci. Eng., 2016, 3(3): 263‒282 https://doi.org/10.15302/J-FASE-2016103

References

[1]
Kang M S, Din A K, Zhang Y, Magari R. Combining ability for rind puncture resistance in maize. Crop Science, 1999, 39(2): 368–371
CrossRef Google scholar
[2]
Mi C, Zhang X, Li S, Yang J, Zhu D, Yang Y. Assessment of environment lodging stress for maize using fuzzy synthetic evaluation. Mathematical and Computer Modelling, 2011, 54(3–4): 1053–1060
CrossRef Google scholar
[3]
Xue J T, Zhang B M, Dong Z Q, Zhao M, Huang C L. Effects of chemical regulation on lodging and yield of maize. Journal of Maize Sciences, 2009, 2: 024
[4]
Rajala A, Peltonen-Sainio P. Plant growth regulator effects on spring cereal root and shoot growth. Agronomy Journal, 2001, 93(4): 936–943
CrossRef Google scholar
[5]
Rajala A, Peltonen-Sainio P, Onnela M, Jackson M. Effects of applying stem-shortening plant growth regulators to leaves on root elongation by seedlings of wheat, oat and barley: mediation by ethylene. Plant Growth Regulation, 2002, 38(1): 51–59
CrossRef Google scholar
[6]
Shekoofa A, Emam Y. Plant growth regulator (ethepon) alters maize (Zea mays L.) growth, water use and grain yield under water stress. Journal of Agronomy, 2008, 7(1): 41–48
CrossRef Google scholar
[7]
Khosravi G R, Anderson I. Growth, yield, and yield components of ethephon-treated corn. Plant Growth Regulation, 1991, 10(1): 27–36
CrossRef Google scholar
[8]
Merchante C, Alonso J M, Stepanova A N. Ethylene signaling: simple ligand, complex regulation. Current Opinion in Plant Biology, 2013, 16(5): 554–560
CrossRef Google scholar
[9]
Habben J E, Bao X, Bate N J, DeBruin J L, Dolan D, Hasegawa D, Helentjaris T G, Lafitte R H, Lovan N, Mo H, Reimann K, Schussler J R. Transgenic alteration of ethylene biosynthesis increases grain yield in maize under field drought-stress conditions. Plant Biotechnology Journal, 2014, 12(6): 685–693
CrossRef Google scholar
[10]
Chen J F, Gallie D R. Analysis of the functional conservation of ethylene receptors between maize and Arabidopsis. Plant Molecular Biology, 2010, 74(4–5): 405–421
CrossRef Google scholar
[11]
Yamauchi T, Watanabe K, Fukazawa A, Mori H, Abe F, Kawaguchi K, Oyanagi A, Nakazono M. Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions. Journal of Experimental Botany, 2014, 65(1): 261–273
CrossRef Google scholar
[12]
Kendrick M D, Chang C. Ethylene signaling: new levels of complexity and regulation. Current Opinion in Plant Biology, 2008, 11(5): 479–485
CrossRef Google scholar
[13]
Stepanova A N, Alonso J M. Ethylene signaling and response: where different regulatory modules meet. Current Opinion in Plant Biology, 2009, 12(5): 548–555
CrossRef Google scholar
[14]
Ma B, Chen S, Zhang J. Ethylene signaling in rice. Chinese Science Bulletin, 2010, 55(21): 2204–2210
CrossRef Google scholar
[15]
Wang F, Cui X, Sun Y, Dong C H. Ethylene signaling and regulation in plant growth and stress responses. Plant Cell Reports, 2013, 32(7): 1099–1109
CrossRef Google scholar
[16]
Gagne J M, Smalle J, Gingerich D J, Walker J M, Yoo S D, Yanagisawa S, Vierstra R D. Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(17): 6803–6808
CrossRef Google scholar
[17]
Qiao H, Chang K N, Yazaki J, Ecker J R. Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes & Development, 2009, 23(4): 512–521
CrossRef Google scholar
[18]
Potuschak T, Vansiri A, Binder B M, Lechner E, Vierstra R D, Genschik P. The exoribonuclease XRN4 is a component of the ethylene response pathway in Arabidopsis. Plant Cell Online, 2006, 18(11): 3047–3057
CrossRef Google scholar
[19]
Yoo S D, Cho Y H, Tena G, Xiong Y, Sheen J. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature, 2008, 451(7180): 789–795
CrossRef Google scholar
[20]
Hahn A, Harter K. Mitogen-activated protein kinase cascades and ethylene: signaling, biosynthesis, or both? Plant Physiology, 2009, 149(3): 1207–1210
CrossRef Google scholar
[21]
Kieber J J, Rothenberg M, Roman G, Feldmann K A, Ecker J R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell, 1993, 72(3): 427–441
CrossRef Google scholar
[22]
Sharp R E, LeNoble M E, Else M A, Thorne E T, Gherardi F. Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene. Journal of Experimental Botany, 2000, 51(350): 1575–1584
CrossRef Google scholar
[23]
Rajala A, Peltonen-Sainio P. Timing applications of growth regulators to alter spring cereal development at high latitudes. Agricultural and Food Science, 2008, 11(3): 233–244
[24]
Azuma T, Hatanaka T, Uchida N, Yasuda T. Interactions between abscisic acid, ethylene and gibberellin in internodal elongation in floating rice: the promotive effect of abscisic acid at low humidity. Plant Growth Regulation, 2003, 41(2): 105–109
CrossRef Google scholar
[25]
LeNoble M E, Spollen W G, Sharp R E. Maintenance of shoot growth by endogenous ABA: genetic assessment of the involvement of ethylene suppression. Journal of Experimental Botany, 2004, 55(395): 237–245
CrossRef Google scholar
[26]
Rzewuski G, Sauter M. Ethylene biosynthesis and signaling in rice. Plant Science, 2008, 175(1–2): 32–42
CrossRef Google scholar
[27]
Ma T L, Wu W H, Wang Y. Transcriptome analysis of rice root responses to potassium deficiency. BMC Plant Biology, 2012, 12(1): 161
CrossRef Google scholar
[28]
Schnable P S, Hochholdinger F, Nakazono M. Global expression profiling applied to plant development. Current Opinion in Plant Biology, 2004, 7(1): 50–56
CrossRef Google scholar
[29]
Zheng J, Fu J J, Gou M Y, Huai J L, Liu Y J, Jian M, Huang Q S, Guo X Y, Dong Z G, Wang H Z, Wang G Y. Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Molecular Biology, 2010, 72(4–5): 407–421
CrossRef Google scholar
[30]
Schachtman D P, Shin R. Nutrient sensing and signaling: NPKS. Annual Review of Plant Biology, 2007, 58(1): 47–69
CrossRef Google scholar
[31]
Van Zhong G, Burns J K. Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Molecular Biology, 2003, 53(1): 117–131
CrossRef Google scholar
[32]
Cheng W H, Chiang M H, Hwang S G, Lin P C. Antagonism between abscisic acid and ethylene in Arabidopsis acts in parallel with the reciprocal regulation of their metabolism and signaling pathways. Plant Molecular Biology, 2009, 71(1–2): 61–80
CrossRef Google scholar
[33]
Hiraga S, Sasaki K, Hibi T, Yoshida H, Uchida E, Kosugi S, Kato T, Mie T, Ito H, Katou S, Seo S, Matsui H, Ohashi Y, Mitsuhara I. Involvement of two rice ETHYLENE INSENSITIVE 3-LIKE genes in wound signaling. Molecular Genetics and Genomics, 2009, 282(5): 517–529
CrossRef Google scholar
[34]
Zhu Y, Fu J J, Zhang J P, Liu T S, Jia Z W, Wang J S, Jin Y, Lian Y, Wang M, Zheng J, Hou W, Wang G Y. Genome-wide analysis of gene expression profiles during ear development of maize. Plant Molecular Biology, 2009, 70(1–2): 63–77
CrossRef Google scholar
[35]
Xing H, Pudake R N, Guo G, Xing G, Hu Z, Zhang Y, Sun Q, Ni Z. Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genomics, 2011, 12(1): 178
CrossRef Google scholar
[36]
Sauter M, Kende H. Gibberellin-induced growth and regulation of the cell division cycle in deepwater rice. Planta, 1992, 188(3): 362–368
CrossRef Google scholar
[37]
van der Knaap E, Kim J H, Kende H. A novel gibberellin-induced gene from rice and its potential regulatory role in stem growth. Plant Physiology, 2000, 122(3): 695–704
CrossRef Google scholar
[38]
Li C, Wong W H. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proceedings of the National Academy of Sciences of the United States of America, 2001, 98(1): 31–36
CrossRef Google scholar
[39]
Livak K J, Schmittgen T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 2001, 25(4): 402–408
CrossRef Google scholar
[40]
Kutschera U, Wang Z Y. Growth-limiting proteins in maize coleoptiles and the auxin-brassinosteroid hypothesis of mesocotyl elongation. Protoplasma, 2015, 253(1): 1–12
[41]
Zhang Q, Cheetamun R, Dhugga K S, Rafalski J A, Tingey S V, Shirley N J, Taylor J, Hayes K, Beatty M, Bacic A, Burton R A, Fincher G B. Spatial gradients in cell wall composition and transcriptional profiles along elongating maize internodes. BMC Plant Biology, 2014, 14(1): 27
CrossRef Google scholar
[42]
Bosch M, Mayer C D, Cookson A, Donnison I S. Identification of genes involved in cell wall biogenesis in grasses by differential gene expression profiling of elongating and non-elongating maize internodes. Journal of Experimental Botany, 2011, 62(10): 3545–3561
CrossRef Google scholar
[43]
Goddemeier M L, Wulff D, Feix G. Root-specific expression of a Zea mays gene encoding a novel glycine-rich protein, zmGRP3. Plant Molecular Biology, 1998, 36(5): 799–802
CrossRef Google scholar
[44]
Matsuyama T, Satoh H, Yamada Y, Hashimoto T. A maize glycine-rich protein is synthesized in the lateral root cap and accumulates in the mucilage. Plant Physiology, 1999, 120(3): 665–674
CrossRef Google scholar
[45]
Lv H, Zheng J, Wang T, Fu J, Huai J, Min H, Zhang X, Tian B, Shi Y, Wang G. The maize d2003, a novel allele of VP8, is required for maize internode elongation. Plant Molecular Biology, 2014, 84(3): 243–257
CrossRef Google scholar
[46]
Zhang Z, Zhang J, Chen Y, Li R, Wang H, Wei J. Genome-wide analysis and identification of HAK potassium transporter gene family in maize (Zea mays L.). Molecular Biology Reports, 2012, 39(8): 8465–8473
CrossRef Google scholar
[47]
Swain S M, Singh D P. Tall tales from sly dwarves: novel functions of gibberellins in plant development. Trends in Plant Science, 2005, 10(3): 123–129
CrossRef Google scholar
[48]
Wang Y, Deng D. Molecular basis and evolutionary pattern of GA-GID1-DELLA regulatory module. Molecular Genetics and Genomics, 2014, 289(1): 1–9
CrossRef Google scholar
[49]
Czechowski T, Bari R P, Stitt M, Scheible W R, Udvardi M K. Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root-and shoot-specific genes. Plant Journal, 2004, 38(2): 366–379
CrossRef Google scholar
[50]
Ma J, Morrow D J, Fernandes J, Walbot V. Comparative profiling of the sense and antisense transcriptome of maize lines. Genome Biology, 2006, 7(3): R22
CrossRef Google scholar
[51]
Liu X, Fu J, Gu D, Liu W, Liu T, Peng Y, Wang J, Wang G. Genome-wide analysis of gene expression profiles during the kernel development of maize (Zea mays L.). Genomics, 2008, 91(4): 378–387
CrossRef Google scholar
[52]
Wilson J, Mertens D. Cell wall accessibility and cell structure limitations to microbial digestion of forage. Crop Science, 1995, 35(1): 251–259
CrossRef Google scholar
[53]
Gou J Y, Wang L J, Chen S P, Hu W L, Chen X Y. Gene expression and metabolite profiles of cotton fiber during cell elongation and secondary cell wall synthesis. Cell Research, 2007, 17(5): 422–434
[54]
Ydenberg C A, Padrick S B, Sweeney M O, Gandhi M, Sokolova O, Goode B L. GMF severs actin-Arp2/3 complex branch junctions by a cofilin-like mechanism. Current Biology, 2013, 23(12): 1037–1045
CrossRef Google scholar
[55]
Levitin B, Richter D, Markovich I, Zik M. Arabinogalactan proteins 6 and 11 are required for stamen and pollen function in Arabidopsis. Plant Journal, 2008, 56(3): 351–363
CrossRef Google scholar
[56]
Anand S, Tyagi A K. Characterization of a pollen-preferential gene OSIAGP from rice (Oryza sativa L. subspecies indica) coding for an arabinogalactan protein homologue, and analysis of its promoter activity during pollen development and pollen tube growth. Transgenic Research, 2010, 19(3): 385–397
CrossRef Google scholar
[57]
Mangeon A, Junqueira R M, Sachetto-Martins G. Functional diversity of the plant glycine-rich proteins superfamily. Plant Signaling & Behavior, 2010, 5(2): 99–104
CrossRef Google scholar
[58]
Gomez J, Sánchez-Martínez D, Stiefel V, Rigau J, Puigdomènech P, Pagès M. A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature, 1988, 334(6179): 262–264.
[59]
Elledge S J. Mitotic arrest: Mad2 prevents sleepy from waking up the APC. Science, 1998, 279(5353): 999–1000
CrossRef Google scholar
[60]
Yu H G, Muszynski M G, Kelly Dawe R. The maize homologue of the cell cycle checkpoint protein MAD2 reveals kinetochore substructure and contrasting mitotic and meiotic localization patterns. Journal of Cell Biology, 1999, 145(3): 425–435
CrossRef Google scholar
[61]
Samac D A, Hironaka C M, Yallaly P E, Shah D M. Isolation and characterization of the genes encoding basic and acidic chitinase in Arabidopsis thaliana. Plant Physiology, 1990, 93(3): 907–914
CrossRef Google scholar
[62]
Collinge D B, Kragh K M, Mikkelsen J D, Nielsen K K, Rasmussen U, Vad K. Plant chitinases. Plant Journal, 1993, 3(1): 31–40
CrossRef Google scholar
[63]
Frey M, Stettner C, Paré P W, Schmelz E A, Tumlinson J H, Gierl A. An herbivore elicitor activates the gene for indole emission in maize. Proceedings of the National Academy of Sciences of the United States of America, 2000, 97(26): 14801–14806
CrossRef Google scholar
[64]
Xia Z, Turner G C, Hwang C S, Byrd C, Varshavsky A. Amino acids induce peptide uptake via accelerated degradation of CUP9, the transcriptional repressor of the PTR2 peptide transporter. Journal ofbiological Chemistry, 2008, 283(43): 28958–28968
CrossRef Google scholar
[65]
Dietrich D, Hammes U, Thor K, Suter ‐ Grotemeyer M, Flückiger R, Slusarenko A J, Ward J M, Rentsch D. AtPTR1, a plasma membrane peptide transporter expressed during seed germination and in vascular tissue of Arabidopsis. Plant Journal, 2004, 40(4): 488–499
CrossRef Google scholar
[66]
Karim S, Holmström K O, Mandal A, Dahl P, Hohmann S, Brader G, Palva E T, Pirhonen M. AtPTR3, a wound-induced peptide transporter needed for defence against virulent bacterial pathogens in Arabidopsis. Planta, 2007, 225(6): 1431–1445
CrossRef Google scholar
[67]
Heller W, Hahlbrock K. Highly purified “flavanone synthase” from parsley catalyzes the formation of naringenin chalcone. Archives of Biochemistry and Biophysics, 1980, 200(2): 617–619
CrossRef Google scholar
[68]
Peer W A, Bandyopadhyay A, Blakeslee J J, Makam S N, Chen R J, Masson P H, Murphy A S. Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell Online, 2004, 16(7): 1898–1911
CrossRef Google scholar
[69]
Franken P, Niesbach-Klösgen U, Weydemann U, Marechal-Drouard L, Saedler H, Wienand U. The duplicated chalcone synthase genes C2 and Whp (white pollen) of Zea mays are independently regulated; evidence for translational control of Whp expression by the anthocyanin intensifying gene in. EMBO Journal, 1991, 10(9): 2605
[70]
Taylor L P, Briggs W R. Genetic regulation and photocontrol of anthocyanin accumulation in maize seedlings. Plant Cell Online, 1990, 2(2): 115–127
CrossRef Google scholar
[71]
Della Vedova C B, Lorbiecke R, Kirsch H, Schulte M B, Scheets K, Borchert L M, Scheffler B E, Wienand U, Cone K C, Birchler J A. The dominant inhibitory chalcone synthase allele C2-Idf (Inhibitor diffuse) from Zea mays (L.) acts via an endogenous RNA silencing mechanism. Genetics, 2005, 170(4): 1989–2002
CrossRef Google scholar
[72]
Wang Y, Li J. Molecular basis of plant architecture. Annual Review of Plant Biology, 2008, 59(1): 253–279
CrossRef Google scholar
[73]
Depuydt S, Hardtke C S. Hormone signalling crosstalk in plant growth regulation. Current Biology, 2011, 21(9): R365–R373
CrossRef Google scholar
[74]
Peer W A. From perception to attenuation: auxin signalling and responses. Current Opinion in Plant Biology, 2013, 16(5): 561–568
CrossRef Google scholar
[75]
Gallie D, Young T. The ethylene biosynthetic and perception machinery is differentially expressed during endosperm and embryo development in maize. Molecular Genetics and Genomics, 2004, 271(3): 267–281
CrossRef Google scholar
[76]
Guo H, Ecker J R. The ethylene signaling pathway: new insights. Current Opinion in Plant Biology, 2004, 7(1): 40–49
CrossRef Google scholar
[77]
Zhang J, Simmons C, Yalpani N, Crane V, Wilkinson H, Kolomiets M. Genomic analysis of the 12-oxo-phytodienoic acid reductase gene family of Zea mays. Plant Molecular Biology, 2005, 59(2): 323–343
CrossRef Google scholar
[78]
Speirs J, Binney A, Collins M, Edwards E, Loveys B. Expression of ABA synthesis and metabolism genes under different irrigation strategies and atmospheric VPDs is associated with stomatal conductance in grapevine (Vitis vinifera L. cv Cabernet Sauvignon). Journal of Experimental Botany, 2013, 64(7): 1907–1916
CrossRef Google scholar
[79]
Fukao T, Bailey-Serres J. Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(43): 16814–16819
CrossRef Google scholar
[80]
Jackson M B. Ethylene-promoted elongation: an adaptation to submergence stress. Annals of Botany, 2008, 101(2): 229–248
CrossRef Google scholar
[81]
Riou-Khamlichi C, Huntley R, Jacqmard A, Murray J A. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science, 1999, 283(5407): 1541–1544
CrossRef Google scholar
[82]
Rupp H M, Frank M, Werner T, Strnad M, Schmülling T. Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristem. Plant Journal, 1999, 18(5): 557–563
CrossRef Google scholar
[83]
Leibfried A, To J P, Busch W, Stehling S, Kehle A, Demar M, Kieber J J, Lohmann J U. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature, 2005, 438(7071): 1172–1175
CrossRef Google scholar
[84]
Fleet C M, Sun T P. A DELLAcate balance: the role of gibberellin in plant morphogenesis. Current Opinion in Plant Biology, 2005, 8(1): 77–85
CrossRef Google scholar
[85]
Wang Y, Deng D, Ding H, Xu X, Zhang R, Wang S, Bian Y, Yin Z, Chen Y. Gibberellin biosynthetic deficiency is responsible for maize dominant Dwarf11 (D11) mutant phenotype: physiological and transcriptomic evidence. PLoS ONE, 2013, 8(6): e66466
CrossRef Google scholar
[86]
Winkler R G, Freeling M. Physiological genetics of the dominant gibberellin-nonresponsive maize dwarfs, Dwarf8 and Dwarf9. Planta, 1994, 193(3): 341–348
CrossRef Google scholar
[87]
Peng J, Carol P, Richards D E, King K E, Cowling R J, Murphy G P, Harberd N P. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes & Development, 1997, 11(23): 3194–3205
CrossRef Google scholar
[88]
Gale M D, Devos K M. Comparative genetics in the grasses. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(5): 1971–1974
CrossRef Google scholar
[89]
Teng F, Zhai L, Liu R, Bai W, Wang L, Huo D, Tao Y, Zheng Y, Zhang Z. ZmGA3ox2, a candidate gene for a major QTL, qPH3. 1, for plant height in maize. Plant Journal, 2013, 73(3): 405–416
CrossRef Google scholar
[90]
Spielmeyer W, Ellis M H, Chandler P M. Semidwarf (sd-1),“green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proceedings of the National Academy of Sciences of the United States of America, 2002, 99(13): 9043–9048
CrossRef Google scholar
[91]
Winkler R G, Helentjaris T. The maize Dwarf3 gene encodes a cytochrome P450-mediated early step in Gibberellin biosynthesis. Plant Cell Online, 1995, 7(8): 1307–1317
CrossRef Google scholar
[92]
Jiang F, Guo M, Yang F, Duncan K, Jackson D, Rafalski A, Wang S, Li B. Mutations in an AP2 transcription factor-like gene affect internode length and leaf shape in maize. PLoS ONE, 2012, 7(5): e37040
CrossRef Google scholar
[93]
Igarashi D, Ishida S, Fukazawa J, Takahashi Y. 14–3-3 proteins regulate intracellular localization of the bZIP transcriptional activator RSG. Plant Cell Online, 2001, 13(11): 2483–2497
CrossRef Google scholar
[94]
Kim J H, Choi D, Kende H. The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant Journal, 2003, 36(1): 94–104
CrossRef Google scholar
[95]
Mockaitis K, Estelle M. Auxin receptors and plant development: a new signaling paradigm. Annual Review of Cell and Developmental Biology, 2008, 24(1): 55–80
CrossRef Google scholar
[96]
Laskowski M J, Williams M E, Nusbaum H C, Sussex I M. Formation of lateral root meristems is a two-stage process. Development, 1995, 121(10): 3303–3310
[97]
Xie Q, Frugis G, Colgan D, Chua N H. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes & Development, 2000, 14(23): 3024–3036
CrossRef Google scholar
[98]
He X J, Mu R L, Cao W H, Zhang Z G, Zhang J S, Chen S Y. AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant Journal, 2005, 44(6): 903–916
CrossRef Google scholar
[99]
Gu L, Liu Y, Zong X, Liu L, Li D P, Li D Q. Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress. Molecular Biology Reports, 2010, 37(8): 4067–4073
CrossRef Google scholar
[100]
Hrabak E M, Chan C W, Gribskov M, Harper J F, Choi J H, Halford N, Kudla J, Luan S, Nimmo H G, Sussman M R. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiology, 2003, 132(2): 666–680
CrossRef Google scholar
[101]
Knöller A S, Blakeslee J J, Richards E L, Peer W A, Murphy A S. Brachytic2/ZmABCB1 functions in IAA export from intercalary meristems. Journal of Experimental Botany, 2010, 61(13): 3689–3696
CrossRef Google scholar
[102]
McLamore E S, Diggs A, Calvo Marzal P, Shi J, Blakeslee J J, Peer W A, Murphy A S, Porterfield D M. Non-invasive quantification of endogenous root auxin transport using an integrated flux microsensor technique. Plant Journal, 2010, 63(6): 1004–1016
CrossRef Google scholar
[103]
Wei X Y, Zhang M C, Li Z H, Duan L S. Differences in responding sensitivity to ethephon among different maize genotypes. Acta Agronomica Sinica, 2011, 37(10): 1819–1827
CrossRef Google scholar
[104]
Wei X Y, Zhang M C, Zhang Y,Li Z H, Duan L S . Effects of ethephon on internode elongation and endogenous hormones in different genotypes of maize. Chinese Journal of Pesticide Science, 2011, 13(5): 475–479
[105]
Werner T, Schmulling T. Cytokinin action in plant development. Current Opinion in Plant Biology, 2009, 12(5): 527–538
CrossRef Google scholar
[106]
Daviere J M, Achard P. Gibberellin signaling in plants. Development, 2013, 140(6): 1147–1151
CrossRef Google scholar

Acknowledgements

This research was supported by the National High Technology Research and Development Program of China (2011AA10A206). The authors thank Prof. Huub J. Speirtz, Wageningen University, for language improvement.

Supplementary materials

The online version of this article at http://dx.doi.org/10.15302/J-FASE-2016103 contains supplementary materials (Appendix A)

Compliance with ethics guidelines

Xiaoyi Wei, Weiqiang Zhang, Qian Zhang, Pei Sun, Zhaohu Li, Mingcai Zhang, Jianmin Li, and Liusheng Duan declare that they have no conflict of interest or financial conflicts to disclose.
This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2016. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)
AI Summary AI Mindmap
PDF(1283 KB)

Accesses

Citations

Detail

Sections
Recommended

/