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ASPHC Baner

Vol. 23 No. 4 (2024)

Articles

Histological, hormonal and metabolic response triggered by N-1-naphthylphthalamic acid-induced stem swelling in Solidago canadensis L.

DOI: https://doi.org/10.24326/asphc.2024.5357
Submitted: March 13, 2024
Published: 2024-09-06

Abstract

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.

References

  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. 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
  13. Friml, J. (2022). Fourteen stations of auxin. Cold Spring Harb. Perspect. Biol., 14, a039859. http://doi.org/10.1101/cshperspect.a039859
  14. 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
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. 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
  41. 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
  42. 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
  43. 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
  44. 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
  45. 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
  46. 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
  47. 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
  48. 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
  49. 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

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