Histological, hormonal and metabolic response triggered by N-1-naphthylphthalamic acid-induced stem swelling in Solidago canadensis L.
Agnieszka Marasek-Ciołakowska
The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0001-9349-2566
Michał Dziurka
Polish Academy of Sciences, The Franciszek Górski Institute of Plant Physiology, Niezapominajek 21, 30-239 Kraków, Polandhttps://orcid.org/0000-0002-8265-6243
Justyna Góraj-Koniarska
The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0001-7667-0279
Urszula Kowalska
The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0003-1806-0493
Joanna Szablińska-Piernik
University of Warmia and Mazury, Department of Botany and Evolutionary Ecology, Plac Łódzki 1, 10-719 Olsztyn, Polandhttps://orcid.org/0000-0003-0265-940X
Marcin Horbowicz
University of Warmia and Mazury, Department of Plant Physiology, Genetics and Biotechnology, Oczapowskiego 1A, 10-719 Olsztyn, Polandhttps://orcid.org/0000-0002-1789-4034
Wiesław Wiczkowski
Polish Academy of Sciences, Department of Chemistry and Biodynamics of Food, Institute of Animal Reproduction and Food Research, Tuwima 10, 10-748 Olsztyn, Polandhttps://orcid.org/0000-0001-6021-5589
Kensuke Miyamoto
Osaka Metropolitan University, Faculty of Liberal Arts, Sciences and Global Education, 1-1 Gakuen-cho, Naka-ku, Sakai, Osaka, 599-8531, JapanJunichi Ueda
Osaka Prefecture University, Department of Biological Science, Graduate School of Science, 1-1 Gakuen-cho, Naka-ku, Sakai, Osaka, 599-8531, Japanhttps://orcid.org/0009-0000-7603-5670
Marian Saniewski
The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Polandhttps://orcid.org/0009-0008-2158-4443
Abstrakt
The effect of N-1-naphthylphthalamic acid (NPA, 5.0%, w/w in lanolin) on the growth of Solidago canadensis (Canadian goldenrod) stem was studied, focusing on histological analyses, comprehensive analyses of phytohormones and polar metabolites. NPA substantially induced stem swelling at and above the application site and stimulated vascular cambium activity around the area of its application. The cambial zone in the swelling part of the stem was twice as wide as that treated with lanolin only (control). The proliferation of cambial cells increased xylem production and, consequently, vascular bundle thickness. A significant enlargement of parenchymatous pith cells and an increased diameter of the pith were also observed. Comprehensive phytohormone analyses revealed that NPA increased the content of indole-3-propionic acid, indole-3-acetic acid, and indole-3-acetyl-aspartic acid in the swelling part of the stem, as well as trans-zeatin riboside. These results suggest that NPA-induced stem swelling depends on the dynamics of changes in aux-in and cytokinin metabolites. Furthermore, the contents of monosaccharides (glucose, fructose and galactose) as well as malic, succinic, fumaric acids, cyclitols and quinic acid derivatives in-creased markedly in the swelling stem. This may indicate that the site of NPA-induced stem swell-ing is a physiological sink for polar metabolites needed for the growth of this tissue. Thus, it seems that auxins, in interaction with cytokinins, regulate the strength of the sink, controlling the transport of polar metabolites into the swelling part of S. canadensis stem.
Słowa kluczowe:
auxin transport inhibitor, Canadian goldenrod, secondary growth, stem swelling, vascular cambium, N-1-naphthylphthalamic acidBibliografia
Abas, L., Kolb, M., Stadlmann, J., Janacek, D.P., Lukic K., Schwechheimer, C., Sazanov, L.A., Mach, L., Friml, J., Hammes, U.Z. (2021). Naphthylphthalamic acid associates with and inhibits PIN auxin transporters. P. Natl. Acad. Sci. USA, 118, e2020857118. http://doi.org/10.1073/pnas.2020857118
Abreu, I.N., Johansson, A.I, Sokołowska, K., Niittyla, T., Sundberg, B., Hvidsten, T.R., Street, N.R., Moritz, T. (2020). A metabolite roadmap of the wood-forming tissue in Populus tremula. New Phytol., 228, 1559–1572. http://doi.org/10.1111/nph.16799
Ahkami, A.H, Melzer, M., Ghaffari, M.R, Pollmann, S., Javid, M.G., Shahinnia, F., Hajirezaei, M.R, Druege, U. (2013). Distribution of indole-3-acetic acid in Petunia hybrida shoot tip cuttings and relationship between auxin transport, carbohydrate metabolism and adventitious root formation. Planta, 238, 499–517. http://doi.org/10.1007/s00425-013-1907-z
Balasubramanian, V.K., Rivas-Ubach, A., Winkler, T., Mitchell, H., Moran, J., Ahkami, A.H. (2023). Modulation of polar auxin transport identifies the molecular determination of source-sink carbon relationships and sink strength in poplar. Tree Physiol., tpad073. http://doi.org/10.1093/treephys/tpad073
Baranová, B., Troščáková-Kerpčárová, E., Grulová, D. (2022). Survey of the Solidago canadensis L. Morpho-logical traits and essential oil production: aboveground biomass growth and abundance of the invasive gold-enrod appears to be reciprocally enhanced within the invaded stands. Plants, 11, 535. http://doi.org/10.3390/plants11040535
Bielecka, A., Królak, E., Biardzka, E. (2017). Habitat conditions of Canadian goldenrod in a selected region of Eastern Poland. J. Ecol. Engineer., 18, 76–81. http://doi.org/10.12911/22998993/74284
Brown, D.E., Rashotte, A.M., Murphy, A.S., Normanly, J., Tague, B.W., Peer, W., Taiz, L., Muday, G.K. (2001). Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol., 126, 524–535. http://doi.org/10.1104/126.2.524
Chen, J.-J., Wang, L.-Y., Immanen, J., Nieminen, K., Spicer, R., Helariutta, Y., Zhang, J., He X.-Q. (2019). Differ-ential regulation of auxin and cytokinin during the secondary vascular tissue regeneration in Populus trees. New Phytol., 224, 188–201. http://doi.org/10.1111/nph.16019
Dębski, H., Wiczkowski, W., Horbowicz, M. (2021). Effect of elicitation with iron chelate and sodium metasili-cate on phenolic compounds in legume sprouts. Molecules, 26, 1345. http://doi.org/10.3390/molecules26051345
Dreger, M., Szalata, M. (2022). The effect of TIBA and NPA on shoot regeneration of Cannabis sativa L. epi-cotyl explants. Agronomy, 12, 104. http://doi.org/10.3390/agronomy12010104
Dziurka, M., Góraj-Koniarska, J., Marasek-Ciolakowska, A., Kowalska, U., Saniewski, M., Ueda, J., Miyamoto, K. (2022). A possible mode of action of methyl jasmonate to induce the secondary abscission zone in stems of Bryophyllum calycinum: relevance to plant hormone dynamics. Plants, 11, 360. http://doi.org/10.3390/plants11030360
Fábregas, N., Formosa-Jordan, P., Confraria, A., Siligato, R., Alonso, J.M., Swarup, R., Bennet, M.J., Máhönen, A.P., Caño-Delgado, I., Ibañes, M. (2015). Auxin influx carriers control vascular patterning and xylem dif-ferentiation in Arabidopsis thaliana. PLoS Genet., 11, e1005183. http://doi.org/10.1371/journal.pgen.1005183
Friml, J. (2022). Fourteen stations of auxin. Cold Spring Harb. Perspect. Biol., 14, a039859. http://doi.org/10.1101/cshperspect.a039859
Gong, W., Long, J., Wu, Y., Du, C., Zhang X., Zhang, J. (2022). Application of NPA restrained leaf expansion by reduced cell division in soybean under stress. J. Plant Growth Regul., 41, 3345–3358. http://doi.org/10.1007/s00344-021-10517-w
Hartig, K., Beck, E. (2006). Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle. Plant Biol., 8, 389–396. http://doi.org/10.1055/s-2006-923797
Hayashi, K., Arai, K., Aoi, Y., Tanaka, Y., Hira, H., Guo, R., Hu, Y., Guo, R., Hu, Y., Ge, C., Zhao, Y., Kasahara, H., Fukui, K. (2021). The main oxidative inactivation pathway of the plant hormone auxin. Nat. Commun., 12, 6752. http://doi.org/10.1038/s41467-021-27020-1
Hu, W., Fagundez, S., Katin-Grazzini, L., Li, Y., Li. W., Chen, Y., Wang, X., Deng, Z., Xie, S., McAvoy, R.J., Li, Y. (2017). Endogenous auxin and its manipulation influence in vitro shoot organogenesis of citrus explants. Hort. Res., 4, 17071. http://doi.org/10.1038/hortres.2017.71
Immanen, J., Nieminen, K., Smolander, O.P., Kojima, M., Alonso Serra, J., Koskinen, P., Zhang, J., Elo, A., Ma-honen, A.P., Street, N., Bhalerao, R.P., Paulin, L., Auvinen, P., Sakakibara, H., Helariutta, Y. (2016). Cytokin-in and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activ-ity. Current Biol., 26, 1990–1997. http://doi.org/10.1016/j.cub.2016.05.053
Johnson, D., Eckart, P., Alsamadisi, N., Noble, H., Martin, C., Spicer, R. (2018). Polar auxin transport is implicat-ed in vessel differentiation and spatial patterning during secondary growth in Populus. Am. J. Bot., 105, 186–196. http://doi.org/10.1002/ajb2.1035
Johnston, C.R., Malladi, A., Vencill, W.K., Grey, T.L., Culpepper, S., Henry, G., Czarnota, M.A., Randell, T.M. (2020). Investigation of physiological and molecular mechanisms conferring diurnal variation in auxinic herbicide efficacy. PloS ONE, 15, e0238144. http://doi.org/10.1371/journal.pone.0238144
Kapusta, G. (1979). Seedbed tillage and herbicide influence on soybean (Glycine max) weed control and yield. Weed Sci., 27, 520–526. http://doi.org/10.1017/S0043174500044520
Kong, M., Liu, X., Sun, L., Tah, S. (2022). Molecular mechanisms of N-1-naphthylphthalamic acid, a chemical tool in plant biology and agriculture. Mol. Hort., 2, 22. http://doi.org/10.1186/s43897-022-00043-y
Korasick, D.A., Enders, T.A., Strader, L.C. (2013). Auxin biosynthesis and storage forms. J. Exp. Bot., 64, 2541–2555. http://doi.org/10.1093/jxb/ert080
Kushwah, S., Jones, A.M., Laxmi, A. (2011). Cytokinin interplay with ethylene, auxin, and glucose signaling controls Arabidopsis seedlings root directional growth. Plant Physiol., 156, 1851–1866. http://doi.org/10.1104/pp.111.175794
Lemoine, R., La Camera, S., Atanassova, R., Dedaldechamp, F., Allario, T., Pourtau, N., Bonnemain, J.-L., Laloi, M., Coutos-Thevenot, P., Maurousset, L., Faucher, M., Girousse, C., Lemonnier, P., Parrilla, J., Durand, M. (2013). Source-to-sink transport of sugar and regulation by environmental factors. Front. Plant Sci., 4, 272. http://doi.org/10.3389/fpls.2013.00272
Little, C.H.A., MacDonald, J.E., Olsson, O. (2002). Involvement of indole-3-acetic acid in fascicular and inter-fascicular cambial growth and interfascicular extraxylary fiber differentiation in Arabidopsis thaliana inflo-rescence stems. Int. Mol. J. Sci., 163, 519–529. http://doi.org/10.1086/339642
Ludwig-Müller, J., 2020. Synthesis and hydrolysis of auxins and their conjugates with different side-chain lengths: Are all products active auxins? Period. Biol., 121, 81–96. http://doi.org/10.18054./pb.v121-122i3-4.10516
Marasek-Ciolakowska, A., Saniewski, M., Dziurka, M., Kowalska, U., Góraj-Koniarska, J, Ueda, J., Miyamoto, K. (2020). Formation of the secondary abscission zone induced by interaction of methyl jasmonate and auxin in Bryophyllum calycinum: relevance to auxin status and histology. Int. J. Mol. Sci., 21, 2784. http://doi.org/10.3390/ijms21082784
Marasek-Ciolakowska, A., Dziurka, M., Kowalska, U., Góraj-Koniarska, J., Saniewski, M., Ueda, J., Miyamoto, K. (2021). Mode of action of 1-N-naphthylphthalamic acid in conspicuous local stem swelling of succulent plant, Bryophyllum calycinum: relevance to the aspects of its histological observation and comprehensive analyses of plant hormones. Int. J. Mol. Sci., 22, 3118. http://doi.org/10.3390/ijms22063118
Matsumoto-Kitano, M., Kusumoto, T., Tarkowski, P., Kinoshita-Tsujimura, K., Vaclavikova, K., Miyawaki, K., Kakimoto, T. (2008). Cytokinins are central regulators of cambial activity. P. Natl. Acad. Sci. USA, 105, 989–1003. http://doi.org/10.1073/pnas.0805619105
Mattsson, J., Sung. Z.R., Berleth, T. (1999). Responses of plant vascular systems to auxin transport inhibition. Development, 126, 2979–2991. http://doi.org/10.1242/dev.126.13.2979
McIntyre, K.E., Bush, D.R., Argueso, C.T. (2021). Cytokinin regulation of source-sink relationships in plant-pathogen interactions. Front. Plant Sci., 12, 677585. http://doi.org/10.3389/fpls.2021.677585
Mishra, B.S., Sharma, M., Laxmi, A. (2022). Role of sugar and auxin crosstalk in plant growth and develop-ment. Physiol. Plant., 174, e13546. http://doi.org/10.1111/ppl.13546
Nongmaithem, S., Devulapalli, S., Sreelakshmi, Y., Sharma, R. (2020). Is naphthylphthalamic acid a specific phytotropin? It elevates ethylene and alters metabolic homeostasis in tomato. Plant Sci., 291, 110358. http://doi.org/10.1016/j.plantsci.2019.110358
Oliveira, P.M.R., Rodrigues, M.A., Goncalves, A.Z. (2019). Exposure of Catasetum fimbriatum aerial roots to light coordinates carbon partitioning between source and sink organs dependent manner. Plant Physiol. Bi-och., 135, 341–347. http://doi.org/10.1016/j.plaphy.2018.12.022
Peer, W.A, Murphy, A.S. (2007). Flavonoids and auxin transport: modulators or regulators?. Trends Plant Sci., 12, 556–563. http://doi.org/10.1016/j.tplants.2007.10.003
Sairanen, I., Novak Pencik, A., Ikeda, Y., Jones B., Sandberg, G., Ljung, K. (2012). Soluble carbohydrates regu-late auxin biosynthesis via PIF proteins in Arabidopsis. Plant Cell, 24, 4907–4916. http://doi.org/10.1105/tpc.112.104794
Segal, L.M., Wightman, F. (1982). Gas chromatographic and GC-MS evidence for the occurrence of 3-indolyl propionic acid and 3-indolylacetic acid in seedlings of Cucurbita pepo. Physiol. Plant., 56, 367–370. http://doi.org/10.1111/j.1399-3054.1982.tb00354.x
Sergeeva, A., Liu, H., Mai, H.-J., Metter-Altmann T., Kiefer, C., Bauer, P. (2021). Cytokinin‐promoted secondary growth and nutrient storage in the perennial stem zone of Arabis alpina. Plant J., 105, 1459–1476. http://doi.org/10.1111/tpj.15123
Strabala, T.J., Wu, Y.H., Li, Y. (1996). Combined effects of auxin transport inhibitors and cytokinin: alterations of organ development in tobacco. Plant Cell Physiol., 37, 1177–1182. http://doi.org/10.1093/oxfordjournals.pcp.a029069
Suer, S., Agusti, J., Sanchez, P, Schwarz, M., Greb, T. (2011). WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell, 23, 3247–3259. http://doi.org/110.1105/tpc.111.087874
Sundberg, B., Tuominen, H., Little, C.H.A. (1994). Effects of the indole-3-acetic-acid (IAA) transport inhibitors N-1-naphthylphthalamic acid and morphactin on endogenous IAA dynamics in relation to compression wood formation in 1-year-old Pinus sylvestris (L.) shoots. Plant Physiol., 106, 469–476. http://doi.org/10.1104/pp.106.2.469
Szablińska-Piernik, J., Lahuta, L.B. (2021). Metabolite profiling of semi-leafless pea (Pisum sativum L.) under progressive soil drought and subsequent re-watering. J. Plant Physiol., 256, 153314. http://doi.org/10.1016/j.jplph.2020.153314
Teale, W., Palme, K. (2018). Naphthylphthalamic acid and the mechanism of polar auxin transport. J. Exp. Bot., 69, 303–312. http://doi.org/10.1093/jxb/erx323
Wang, L., Ruan, Y.-L. (2013). Regulation of cell division and expansion by sugar and auxin signaling. Front. Plant Sci., 4, 163. http://doi.org/10.3389/fpls.2013.00163
Yamaguchi, K., Itoh, T., Shimaji, K. (1980). Compression wood induced by 1-N-naphthylphthalamic acid (NPA) an IAA transport inhibitor. Wood Sci. Technol., 14, 181–185. http://doi.org/10.1007/BF00350568
Zhang, J., Peer, W.A. (2017). Auxin homeostasis: the DAO of catabolism. J. Exp. Bot., 68, 3145–3154. https://doi.org/10.1093/jxb/erx221
Zhang, J., Nieminen, K., Serra, J.A.A., Helariutta, Y. (2014). The formation of wood and its control. Curr. Opin. Plant Biol., 17, 56–63. http://doi.org/10.1016/j.pbi.2013.11.003
Zhong, R., Ye, Z.H. (2001). Alteration of auxin polar transport in the Arabidopsis ifl1 mutants. Plant Physiol., 126, 549–563. http://doi.org/10.1104/pp.126.2.549
The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland https://orcid.org/0000-0001-9349-2566
Polish Academy of Sciences, The Franciszek Górski Institute of Plant Physiology, Niezapominajek 21, 30-239 Kraków, Poland https://orcid.org/0000-0002-8265-6243
The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland https://orcid.org/0000-0001-7667-0279
The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland https://orcid.org/0000-0003-1806-0493
University of Warmia and Mazury, Department of Botany and Evolutionary Ecology, Plac Łódzki 1, 10-719 Olsztyn, Poland https://orcid.org/0000-0003-0265-940X
University of Warmia and Mazury, Department of Plant Physiology, Genetics and Biotechnology, Oczapowskiego 1A, 10-719 Olsztyn, Poland https://orcid.org/0000-0002-1789-4034
Polish Academy of Sciences, Department of Chemistry and Biodynamics of Food, Institute of Animal Reproduction and Food Research, Tuwima 10, 10-748 Olsztyn, Poland https://orcid.org/0000-0001-6021-5589
Osaka Metropolitan University, Faculty of Liberal Arts, Sciences and Global Education, 1-1 Gakuen-cho, Naka-ku, Sakai, Osaka, 599-8531, Japan
Osaka Prefecture University, Department of Biological Science, Graduate School of Science, 1-1 Gakuen-cho, Naka-ku, Sakai, Osaka, 599-8531, Japan https://orcid.org/0009-0000-7603-5670
The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland https://orcid.org/0009-0008-2158-4443
Licencja
![Creative Commons License](http://i.creativecommons.org/l/by/4.0/88x31.png)
Utwór dostępny jest na licencji Creative Commons Uznanie autorstwa 4.0 Międzynarodowe.
Artykuły są udostępniane na zasadach CC BY 4.0 (do 2021 r. na zasadach CC BY-NC-ND 4.0 międzynarodowe).
Przysłanie artykułu do redakcji oznacza, że nie był on opublikowany wcześniej i nie jest rozpatrywany do publikacji gdzie indziej.
Autor podpisuje oświadczenie o oryginalności dzieła, wkładzie poszczególnych osób i źródle finansowania.