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Subcellular localization of endogenous IAA during poplar leaf rhizogenesis revealed by in situ immunocytochemistry

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Abstract

Poplar 741 [Populus alba × (P. davidiana + P. simonii) × P. tomentosa] leaves were rooted within 8 days when cultured on 1/2 MS medium. The subcellular localization of endogenous indole-3-acetic acid (IAA) in the rhizogenesis was investigated, using an immunocytochemical approach. The results of IAA subcellular localization revealed organelle-specific distribution. Three days after root induction, IAA in vascular cambium cells of the basal region of the petiole was distributed mainly in the plasma membrane, endoplasmic reticulum (ER), and nucleus, with a lesser amount in the cytoplasm. In phloem of the basal region of the petiole, IAA was detected in the plasma membrane and ER of the companion cell and in the plasma membrane of the sieve element. In xylem of the basal region of the petiole, no IAA gold particles were labeled. In mesophyll cells IAA was distributed in the chloroplast starch grains before root induction, and the amount in the chloroplast starch grains increased after 3 days after root induction. This suggests that the plasma membrane and nucleus of cambium cells may be the target sites where IAA performs its physiological activities during poplar leaf rhizogenesis. IAA polar transport from lamina mesophyll to the basal region of the petiole during rhizogenesis is mediated by phloem. The starch grains of mesophyll chloroplasts appeared to accumulate IAA and may be a source of IAA during poplar leaf rhizogenesis. Novel and direct evidence regarding the function of IAA during rhizogenesis is provided in this study.

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References

  • Avsian-Kretchmer O, Cheng JC, Chen L, Moctezuma E, Sung ZR (2002) Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny. Plant Physiol 130:199–209

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bainbridge K, Guyomarc’h S, Bayer E, Swarup R, Bennett M, Mandel T, Kuhlemeier C (2008) Auxin influx carriers stabilize phyllotactic patterning. Genes Dev 22:810–823

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Blakesley D (1994) Auxin metabolism and adventitious root initiation. In: Davis TD, Haissig BE (eds) Biology of adventitious root formation. Plenum Press, New York, pp 143–154

    Chapter  Google Scholar 

  • Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, Vernoux T (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482:103–106

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Ren Y, Deng Y, Zhao J (2010) Auxin polar transport is essential for the development of zygote and embryo in Nicotiana tabacum L. and correlated with ABP1 and PM H+-ATPase activities. J Exp Bot 61:1853–1867

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen D, Zhao J (2008) Free IAA in stigmas and styles during pollen germination and pollen tube growth of Nicotiana tabacum. Physiol Plant 134:202–215

    Article  PubMed  CAS  Google Scholar 

  • Cooper WC (1935) Hormones in relation to root formation on stem cuttings. Plant Physiol 10:789–794

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Correa LR, Stein RJ, Fett-Neto AG (2012) Adventitious rooting of detached Arabidopsis thaliana leaves. Biol Plant 56:581–584

    Article  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  PubMed  CAS  Google Scholar 

  • Dong NG, Pei D, Yin WL (2012) Tissue-specific localization and dynamic changes of endogenous IAA during poplar leaf rhizogenesis revealed by in situ immunohistochemistry. Plant Biotechnol Rep 6:165–174

    Article  Google Scholar 

  • Dong NG, Wang QM, Zhang JP, Pei D (2011) Immunohistochemical localization of indole-3-acetic acid during induction of adventitious root formation from cotyledon explants of walnut. J Am Soc Hortic Sci 136:315–319

    CAS  Google Scholar 

  • Falasca G, Zaghi D, Possenti M, Altamura MM (2004) Adventitious root formation in Arabidopsis thaliana thin cell layers. Plant Cell Rep 23:17–25

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Jones AR (2010) Endoplasmic reticulum: the rising compartment in auxin biology. Plant Physiol 154:458–462

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gangopadhyay M, Chakraborty D, Dewanjee S, Bhattacharya S (2010) Clonal propagation of Zephyranthes grandiflora using bulbs as explants. Bio Plant 54:793–797

    Article  Google Scholar 

  • Gatineau F, Fouche JG, Kevers C, Hausman JF, Gaspar T (1997) Quantitative variations of indolyl compounds including IAA, IAA-aspartate and serotonin in walnut microcuttings during root induction. Biol Plant 39:131–137

    Article  CAS  Google Scholar 

  • Han X, Hyun TK, Zhang M, Kumar R, Koh EJ, Kang BH, Lucas WJ, Kim JY (2014) Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Dev Cell 28:132–146

    Article  PubMed  CAS  Google Scholar 

  • Hou ZX, Huang WD (2005) Immunohistochemical localization of IAA and ABP1 in strawberry shoot apexes during floral induction. Planta 222:678–687

    Article  PubMed  CAS  Google Scholar 

  • Jones AM, Im KH, Savka MA, Wu MJ, DeWitt NG, Shillito R, Binns AN (1998) Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science 282:1114–1117

    Article  PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  PubMed  CAS  Google Scholar 

  • Kriechbaumer V, Weigang L, Fiesselmann A, Letzel T, Frey M, Gierl A, Glawischnig E (2008) Characterisation of the tryptophan synthase alpha subunit in maize. BMC Plant Biol 8:44. doi:10.1186/1471-2229-8-44

    Article  PubMed  PubMed Central  Google Scholar 

  • Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28:465–474

    Article  PubMed  CAS  Google Scholar 

  • Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17:1090–1104

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ludwig-Muller J, Vertocnik A, Town CD (2005) Analysis of indole-3-butyric acid-induced adventitious root formation on Arabidopsis stem segments. J Exp Bot 56:2095–2105

    Article  PubMed  Google Scholar 

  • McQueen-Mason SJ, Hamilton RH (1989) The biosynthesis of indole-3-acetic acid from d-tryptophan in Alaska pea plastids. Plant Cell Physiol 30:999–1005

    CAS  Google Scholar 

  • Mertens R, Eberle J, Arnscheidt A, Ledebur A, Weiler EW (1985) Monoclonal antibodies to plant growth regulators. II. Indole-3-acetic acid. Planta 166:389–393

    Article  PubMed  CAS  Google Scholar 

  • Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80

    Article  PubMed  CAS  Google Scholar 

  • Moctezuma E (1999) Changes in auxin patterns in developing gynophores of the peanut plant (Arachis hypogaea L.). Ann Bot 83:235–242

    Article  PubMed  CAS  Google Scholar 

  • Mravec J, Skupa P, Bailly A, Hoyerova K, Krecek P, Bielach A, Petrasek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerova K, Rolcik J, Seifertova D, Luschnig C, Benkova E, Zazimalova E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140

    Article  PubMed  CAS  Google Scholar 

  • Nishimura T, Toyooka K, Stato M, Matsumoto S, Lucas MM, Strnad M, Baluska F, Koshiba T (2011) Immunohistochemical observation of indole-3-acetic acid at the IAA synthetic maize coleoptile tips. Plant Signal Behav 6:2013–2022

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nourissier S, Monteuuis O (2008) In vitro rooting of two Eucalyptus urophylla × Eucalyptus grandis mature clones. In Vitro Cell Dev Biol Plant 44:263–272

    Article  CAS  Google Scholar 

  • Ohmiya A, Hayashi T, Kakiuchi N (1990) Immuno-gold localization of indole-3-acetic acid in peach seedlings. Plant Cell Physiol 31:711–715

    CAS  Google Scholar 

  • Perbal G, Leroux Y, Driss-Ecole D (1982) Mise en evidence de I’AIA-5-3H par autoadiographie dans le coleoptile de Bie. Physiol Plant 54:167–173

    Article  CAS  Google Scholar 

  • Petrásek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688

    Article  PubMed  Google Scholar 

  • Petrásek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D, Wisniewska J, Tadele Z, Kubes M, Covanová M, Dhonukshe P, Skupa P, Benková E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazímalová E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918

    Article  PubMed  Google Scholar 

  • Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21:1659–1668

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Quint M, Gray WM (2006) Auxin signaling. Curr Opin Plant Biol 9:448–453

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schwalm K, Aloni R, Langhans M, Heller W, Stich S, Ullrich CI (2003) Flavonoid-related regulation of auxin accumulation in Agrobacterium tumefaciens-induced plant tumors. Planta 218:163–178

    Article  PubMed  CAS  Google Scholar 

  • Shi L, Miller I, Moore R (1993) Immunocytochemical localization of indole-3-acetic acid in primary root of Zea mays. Plant Cell Environ 16:967–973

    Article  CAS  Google Scholar 

  • Shimomura S, Watanabe S, Ichikawa H (1999) Characterization of auxin-binding protein 1 from tobacco: content, localization and auxin-binding activity. Planta 209:118–125

    Article  PubMed  CAS  Google Scholar 

  • Shishova M, Lindberg S (2010) A new perspective on auxin perception. J Plant Physiol 167:417–422

    Article  PubMed  CAS  Google Scholar 

  • Sun YP, Zhang DL, Smagula J (2010) Micropropagation of Ilex glabra (L.) A. Gray. HortScience 45:805–808

    Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Wisniewska J, Xu J, Seifertová D, Brewer PB, Ruzicka K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883

    Article  PubMed  CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    Article  PubMed  CAS  Google Scholar 

  • Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Qi JY, Ye MB, Shen WB (2008) The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiol 148:881–893

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16:1123–1127

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We sincerely thank Dr. Junzhen Jia and Haihong Liu (College of Biological Sciences, China Agricultural University, China) and Dr. Zhixia Hou (School of Forestry, Beijing Forestry University, China) for their kind help with the experimental methods and equipment. This work was supported by the National Natural Science Foundation of China (grant no. 31171933).

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Authors and Affiliations

  1. Institute of Forestry and Pomology, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100093, People’s Republic of China

    Ningguang Dong & Yanbin Hao

  2. Research Institute of Forestry, Chinese Academy of Forestry, Wan Shou Shan Hou, Haidian District, Beijing, 100091, People’s Republic of China

    Ningguang Dong, Ying Gao & Dong Pei

  3. College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Ningguang Dong & Weilun Yin

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  1. Ningguang Dong
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Correspondence to Dong Pei.

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Dong, N., Gao, Y., Hao, Y. et al. Subcellular localization of endogenous IAA during poplar leaf rhizogenesis revealed by in situ immunocytochemistry. Plant Biotechnol Rep 8, 377–386 (2014). https://doi.org/10.1007/s11816-014-0327-2

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