Red Light Controls Adventitious Root Regeneration by Modulating Hormone Homeostasis in Picea abies Seedlings
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
33014006
PubMed Central
PMC7509059
DOI
10.3389/fpls.2020.586140
Knihovny.cz E-zdroje
- Klíčová slova
- Picea abies, adventitious roots, auxin, conifers, cytokinins, jasmonate, red light, root development,
- Publikační typ
- časopisecké články MeSH
Vegetative propagation relies on the capacity of plants to regenerate de novo adventitious roots (ARs), a quantitative trait controlled by the interaction of endogenous factors, such as hormones and environmental cues among which light plays a central role. However, the physiological and molecular components mediating light cues during AR initiation (ARI) remain largely elusive. Here, we explored the role of red light (RL) on ARI in de-rooted Norway spruce seedlings. We combined investigation of hormone metabolism and gene expression analysis to identify potential signaling pathways. We also performed extensive anatomical characterization to investigate ARI at the cellular level. We showed that in contrast to white light, red light promoted ARI likely by reducing jasmonate (JA) and JA-isoleucine biosynthesis and repressing the accumulation of isopentyl-adenine-type cytokinins. We demonstrated that exogenously applied JA and/or CK inhibit ARI in a dose-dependent manner and found that they possibly act in the same pathway. The negative effect of JA on ARI was confirmed at the histological level. We showed that JA represses the early events of ARI. In conclusion, RL promotes ARI by repressing the accumulation of the wound-induced phytohormones JA and CK.
Department of Biology College of Science for Women Baghdad University Baghdad Iraq
Institut Jean Pierre Bourgin INRAE AgroParisTech Université Paris Saclay Versailles France
Umeå Plant Science Centre Department of Plant Physiology Umeå University Umeå Sweden
Zobrazit více v PubMed
Abarca D., Díaz-Sala C. (2009). “Adventitious root formation in conifers,” in Adventitious Root Formation of Forest Trees and Horticultural Plants – from Genes to Applications. Eds. Niemi K., Scagel C. (Kerala, India: Research Signpost Publishers; ).
Agulló-Antón M.Á., Sánchez-Bravo J., Acosta M., Druege U. (2011). Auxins or Sugars: What Makes the Difference in the Adventitious Rooting of Stored Carnation Cuttings? J. Plant Growth Regul. 30, 100–113. 10.1007/s00344-010-9174-8 DOI
Alallaq S., Ranjan A., Brunoni F., Novák O., Lakehal A., Bellini C. (2020). Red light controls adventitious root regeneration by modulating hormone homeostasis in Picea abies seedlings. BioRxiv. 10.1101/2020.03.11.985838 PubMed DOI PMC
Antoniadi I., Plačková L., Simonovik B., Doležal K., Turnbull C., Ljung K., et al. (2015). Cell-type-specific cytokinin distribution within the arabidopsis primary root apex. Plant Cell 27, 1955–1967. 10.1105/tpc.15.00176 PubMed DOI PMC
Baque M. A., Hahn E.-J., Paek K.-Y. (2010). Induction mechanism of adventitious root from leaf explants of Morinda citrifolia as affected by auxin and light quality. Vitr. Cell. Dev. Biol. - Plant 46, 71–80. 10.1007/s11627-009-9261-3 DOI
Baraldi R., Rossi F., Lercari B. (1988). In vitro shoot development of Prunus GF 655–2: interaction between light and benzyladenine. Physiol. Plant 74, 440–443. 10.1111/j.1399-3054.1988.tb02000.x DOI
Bellini C., Pacurar D., II, Perrone I. (2014). Adventitious Roots and Lateral Roots: Similarities and Differences. Annu. Rev. Plant Biol. 65, 639–666. 10.1146/annurev-arplant-050213-035645 PubMed DOI
Bollmark M., Eliasson L. (1990). A rooting inhibitor present in Norway spruce seedlings grown at high irradiance - a putative cytokinin. Physiol. Plant 80, 527–533. 10.1111/j.1399-3054.1990.tb05674.x DOI
Burescu L., Cachita D., Craciun C. (2015). The effect of different wavelengths LED lighting on the growth of spruce (Picea abies L) plantlets. Rom. Biotechnol. Lett. 20, 11025–11034.
Cai H., Yang C., Liu S., Qi H., Wu L., Xu L. A., et al. (2019). MiRNA-target pairs regulate adventitious rooting in Populus: a functional role for miR167a and its target Auxin response factor 8. Tree Physiol. 39, 1922–1936. 10.1093/treephys/tpz085 PubMed DOI
Campos M. L., Yoshida Y., Major I. T., De Oliveira Ferreira D., Weraduwage S. M., Froehlich J. E., et al. (2016). Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat. Commun. 7, 1–10. 10.1038/ncomms12570 PubMed DOI PMC
Chini A., Fonseca S., Fernández G., Adie B., Chico J. M., Lorenzo O., et al. (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666–671. 10.1038/nature06006 PubMed DOI
Christiaens A., Gobin B., Van Labeke M. C. (2016). “Light quality and adventitious rooting: a mini-review,” in Proc. VIII Int. Symp. on Light in Horticulture. Ed. Currey C. J., et al., Acta Hortic 1134. International Society for Horticultural Science 2016. 10.17660/ActaHortic.2016.1134.50 DOI
Daud N., Faizal A., Geelen D. (2013). Adventitious rooting of Jatropha curcas L. @ is stimulated by phloroglucinol and by red LED light. Vitr. Cell. Dev. Biol. - Plant 49, 183–190. 10.1007/s11627-012-9486-4 DOI
de Wit M., Galvão V. C., Fankhauser C. (2016). Light-Mediated Hormonal Regulation of Plant Growth and Development. Annu. Rev. Plant Biol. 67, 513–537. 10.1146/annurev-arplant-043015-112252 PubMed DOI
Diaz-Sala C., Hutchison K. W., Goldfarb B., Greenwood M. S. (1996). Maturation-related loss in rooting competence by loblolly pine stem cuttings: The role of auxin transport, metabolism and tissue sensitivity. Physiol. Plant 97, 481–490. 10.1034/j.1399-3054.1996.970310.x DOI
Druart P., Kevers C., Boxus P., Gaspar T. (1982). In vitro Promotion of Root Formation by Apple Shoots Through Darkness Effect on Endogenous Phenols and Peroxidases. Z. für Pflanzenphysiol. 108, 429–436. 10.1016/S0044-328X(82)80168-2 DOI
Fett-Neto A. G., Fett J. P., Vieira Goulart L. W., Pasquali G., Termignoni R. R., Ferreira A. G. (2001). Distinct effects of auxin and light on adventitious root development in Eucalyptus saligna and Eucalyptus globulus. Tree Physiol. 21, 457–464. 10.1093/treephys/21.7.457 PubMed DOI
Floková K., Tarkowská D., Miersch O., Strnad M., Wasternack C., Novák O. (2014). UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry 105, 147–157. 10.1016/j.phytochem.2014.05.015 PubMed DOI
Fuernkranz H. A., Nowak C. A., Maynard C. A. (1990). Light effects on in vitro adventitious root formation in axillary shoots of mature Prunus serotina. Physiol. Plant 80, 337–341. 10.1111/j.1399-3054.1990.tb00050.x DOI
Gabryszewska E., Rudnicki R. M. (1997). The effects of light quality on the growth and development of shoots and roots of Ficus benjamina in vitro. Acta Hortic. 418, 163–168. 10.17660/ActaHortic.1997.418.22 DOI
Geiss G., Gutierrez L., Bellini C. (2018). Adventitious Root Formation: New Insights and Perspectives. Root Dev. 37, 127–156. 10.1002/9781444310023.ch5 DOI
Gutierrez L., Bussell J. D., Pǎcurar D., II, Schwambach J., Pǎcurar M., Bellini C. (2009). Phenotypic plasticity of adventitious rooting in arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21, 3119–3132. 10.1105/tpc.108.064758 PubMed DOI PMC
Gutierrez L., Mongelard G., Floková K., Păcurar D., II, Novák O., Staswick P., et al. (2012). Auxin Controls Arabidopsis Adventitious Root Initiation by Regulating Jasmonic Acid Homeostasis. Plant Cell 24, 2515–2527. 10.1105/tpc.112.099119 PubMed DOI PMC
Hamann T., Smets E., Lens F. (2011). A comparison of paraffin and resin-based techniques used in bark anatomy. Taxon 60, 841–851. 10.1002/tax.603016 DOI
Hammerschlag F. A., Bauchan G. R., Scorza R. (1987). Factors influencing in vitro multiplication and rooting of peach cultivars. Plant Cell. Tissue Organ Cult. 8, 235–242. 10.1007/BF00040950 DOI
Iacona C., Muleo R. (2010). Light quality affects in vitro adventitious rooting and ex vitro performance of cherry rootstock Colt. Sci. Hortic. (Amsterdam). 125, 630–636. 10.1016/j.scienta.2010.05.018 DOI
Jarvis B. C., Shaheed A., II (1987). Adventitious root formation in relation to irradiance and auxin supply. Biol. Plant 29, 321–333. 10.1007/BF02886608 DOI
Kazan K., Manners J. M. (2011). The interplay between light and jasmonate signalling during defence and development. J. Exp. Bot. 62, 4087–4100. 10.1093/jxb/err142 PubMed DOI
Klopotek Y., Haensch K. T., Hause B., Hajirezaei M. R., Druege U. (2010). Dark exposure of petunia cuttings strongly improves adventitious root formation and enhances carbohydrate availability during rooting in the light. J. Plant Physiol. 167, 547–554. 10.1016/j.jplph.2009.11.008 PubMed DOI
Klopotek Y., Franken P., Klaering H.-P., Fischer K., Hause B., Hajirezaei M.-R., et al. (2016). A higher sink competitiveness of the rooting zone and invertases are involved in dark stimulation of adventitious root formation in Petunia hybrida cuttings. Plant Sci. 243, 10–22. 10.1016/j.plantsci.2015.11.001 PubMed DOI
Lakehal A., Bellini C. (2019). Control of adventitious root formation: insights into synergistic and antagonistic hormonal interactions. Physiol. Plant 165, 90–100. 10.1111/ppl.12823 PubMed DOI
Lakehal A., Chaabouni S., Cavel E., Le Hir R., Ranjan A., Raneshan Z., et al. (2019. a). A Molecular Framework for the Control of Adventitious Rooting by TIR1/AFB2-Aux/IAA-Dependent Auxin Signaling in Arabidopsis. Mol. Plant 12, 1499–1514. 10.1016/j.molp.2019.09.001 PubMed DOI
Lakehal A., Dob A., Novák O., Bellini C. (2019. b). A DAO1-Mediated Circuit Controls Auxin and Jasmonate Crosstalk Robustness during Adventitious Root Initiation in Arabidopsis. Int. J. Mol. Sci. 20, 4428. 10.3390/ijms20184428 PubMed DOI PMC
Lakehal A., Dob A., Rahneshan Z., Novák O., Escamez S., Alallaq S., et al. (2020. a). ETHYLENE RESPONSE FACTOR 115 integrates jasmonate and cytokinin signaling machineries to repress adventitious rooting in Arabidopsis. New Phytol., nph.16794. 10.1111/nph.16794 PubMed DOI
Lakehal A., Ranjan A., Bellini C. (2020. b). “Multiple Roles of Jasmonates in Shaping Rhizotaxis: Emerging Integrators,” in Jasmonate in Plant Biology. Methods in Molecular Biology, Eds. Champion A and Laplaze L (Humana, New York, NY: ), 2085. 10.1007/978-1-0716-0142 PubMed DOI
Lindroth A. M., Kvarnheden A., von Arnold S. (2001. a). Isolation of a PSTAIRE CDC2 cDNA from Pinus contorta and its expression during adventitious root development. Plant Physiol. Biochem. 39, 107–114. 10.1016/S0981-9428(00)01229-8 DOI
Lindroth A. M., Saarikoski P., Flygh G., Clapham D., Grönroos R., Thelander M., et al. (2001. b). Two S-adenosylmethionine synthetase-encoding genes differentially expressed during adventitious root development in Pinus contorta . Plant Mol. Biol. 46, 335–346. 10.1023/A:1010637012528 PubMed DOI
Liu X., Cohen J. D., Gardner G. (2011). Low-fluence red light increases the transport and biosynthesis of auxin. Plant Phys. 157, 891–904. 10.1104/pp.111.181388 PubMed DOI PMC
Lorenzo O., Chico J. M., Sánchez-Serrano J. J., Solano R. (2004). JASMONATE-INSENSITIVE1 Encodes a MYC Transcription Factor Essential to Discriminate between Different Jasmonate-Regulated Defense Responses in Arabidopsis. Plant Cell 16, 1938–1950. 10.1105/tpc.022319 PubMed DOI PMC
Mao J., Zhang D., Meng Y., Li K., Wang H., Han M. (2019). Inhibition of adventitious root development in apple rootstocks by cytokinin is based on its suppression of adventitious root primordia formation. Physiol. Plant 166, 663–676. 10.1111/ppl.12817 PubMed DOI
McAdam S. A. M., Brodribb T. J., Ross J. J. (2016). Shoot-derived abscisic acid promotes root growth. Plant Cell Environ. 39, 652–659. 10.1111/pce.12669 PubMed DOI
Meng L., Song W., Liu S., Dong J., Zhang Y., Wang C., et al. (2015). Light quality regulates lateral root development in tobacco seedlings by shifting auxin distributions. J. Plant Growth Regul. 34, 574–583. 10.1007/s00344-015-9491-z DOI
Mølmann J. A., Junttila O., Johnsen Ø., Olsen J. E. (2006). Effects of red, far-red and blue light in maintaining growth in latitudinal populations of Norway spruce (Picea abies). Plant Cell Environ. 29, 166–172. 10.1111/j.1365-3040.2005.01408.x PubMed DOI
Mortensen L. M., Sandvik M. (1988). Light quality and growth of Norway spruce (Picea abies (L.)). New For. 2, 281–287. 10.1007/BF00027944 DOI
Nystedt B., Street N. R., Wetterbom A., Zuccolo A., Lin Y.-C., Scofield D. G., et al. (2013). The Norway spruce genome sequence and conifer genome evolution. Nature 497, 579–584. 10.1038/nature12211 PubMed DOI
OuYang F., Mao J.-F., Wang J., Zhang S., Li Y. (2015). Transcriptome Analysis Reveals that Red and Blue Light Regulate Growth and Phytohormone Metabolism in Norway Spruce [Picea abies (L.) Karst.]. PLoS One 10, e0127896. 10.1371/journal.pone.0127896 PubMed DOI PMC
Poudel P. R., Kataoka I., Mochioka R. (2008). Effect of red- and blue-light-emitting diodes on growth and morphogenesis of grapes. Plant Cell. Tissue Organ Cult. 92, 147–153. 10.1007/s11240-007-9317-1 DOI
Ramírez-Carvajal G. A., Morse A. M., Dervinis C., Davis J. M. (2009). The cytokinin type-B response regulator PtRR13 is a negative regulator of adventitious root development in Populus. Plant Physiol. 150, 759–771. 10.1104/pp.109.137505 PubMed DOI PMC
Rhee S. Y., Birnbaum K. D., Ehrnhardt D. W. (2019). Towards Building a Plant Cell Atlas. Trends Plant Sci. 24, 303–310. 10.1016/j.tplants.2019.01.006 PubMed DOI PMC
Ricci A., Rolli E., Dramis L., Diaz-Sala C. (2008). N,N′-bis-(2,3-Methylenedioxyphenyl)urea and N,N′-bis-(3,4-methylenedioxyphenyl)urea enhance adventitious rooting in Pinus radiata and affect expression of genes induced during adventitious rooting in the presence of exogenous auxin. Plant Sci. 175, 356–363. 10.1016/j.plantsci.2008.05.009 DOI
Rittenberg D., Foster L. (1940). A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. J. Biol. Chem. 133, 737–744.
Ruedell C. M., de Almeida M. R., Fett-Neto A. G. (2015). Concerted transcription of auxin and carbohydrate homeostasis-related genes underlies improved adventitious rooting of microcuttings derived from far-red treated Eucalyptus globulus Labill mother plants. Plant Physiol. Biochem. 97, 11–19. 10.1016/j.plaphy.2015.09.005 PubMed DOI
Sassi M., Wang J., Ruberti I., Vernoux T., Xu J. (2013). Shedding light on auxin movement. Light-regulation of polar auxin transport in the photocontrol of plant development. Plant Signaling Behav. 8, 3. 10.4161/psb.23355 PubMed DOI PMC
Steffens B., Rasmussen A. (2016). The Physiology of Adventitious Roots. Plant Physiol. 170, 603–617. 10.1104/pp.15.01360 PubMed DOI PMC
Steffens B., Wang J., Sauter M. (2006). Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223, 604–612. 10.1007/s00425-005-0111-1 PubMed DOI
Stenzel I., Otto M., Delker C., Kirmse N., Schmidt D., Miersch O., et al. (2012). ALLENE OXIDE CYCLASE (AOC) gene family members of Arabidopsis thaliana: tissue- and organ-specific promoter activities and in vivo heteromerization*. J. Exp. Bot. 63, 6125–6138. 10.1093/jxb/ers261 PubMed DOI PMC
Stevens M. E., Woeste K. E., Pijut P. M. (2018). Localized gene expression changes during adventitious root formation in black walnut (Juglans nigra L.). Tree Physiol. 38, 877–894. 10.1093/treephys/tpx175 PubMed DOI
Strömquist L.-H., Eliasson L. (1979). Light inhibition of rooting in Norway spruce ( Picea abies ) cuttings. Can. J. Bot. 57, 1314–1316. 10.1139/b79-160 DOI
Svačinová J., Novák O., Plačková L., Lenobel R., Holík J., Strnad M., et al. (2012). A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods 8, 1–14. 10.1186/1746-4811-8-17 PubMed DOI PMC
Thines B., Katsir L., Melotto M., Niu Y., Mandaokar A., Liu G., et al. (2007). JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661–665. 10.1038/nature05960 PubMed DOI
Xie D. X., Feys B. F., James S., Nieto-Rostro M., Turner J. G. (1998). COI1: An Arabidopsis gene required for jasmonate-regulated defense and fertility. Sci. (80-. ). 280, 1091–1094. 10.1126/science.280.5366.1091 PubMed DOI
Yan Y., Stolz S., Chételat A., Reymond P., Pagni M., Dubugnon L., et al. (2007). A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19, 2470–2483. 10.1105/tpc.107.050708 PubMed DOI PMC
High-throughput interspecies profiling of acidic plant hormones using miniaturised sample processing
Plant Growth Regulators in Tree Rooting