Symplastic transport participation of auxins during plant development
DOI:
https://doi.org/10.29059/cienciauat.v18i2.1833Keywords:
auxins, callose, plant development, plasmodesmata, symplastic transportAbstract
The appropriate organogenesis of plants during their life cycle promotes their development and adaptation to different environmental conditions. Various phytohormones regulate plant development but auxin, called Indole-3-Acetic Acid (IAA), is one of the most important. IAA is synthesized in the aerial part of plant and is mobilized to the demanding tissues by a rapid transport using the phloem and by the polar auxin transport (PAT). Recently, it has been shown that auxins also are mobilized by a symplastic transport (ST) through plasmodesmata (PD), which opening or closing is regulated by the callose degradation or deposition respectively. The objective of the present work was to deepen the analysis on the participation of symplastic transport of auxins during plant development, as well in the callose degradation or deposition, in the closing or opening of the PD, that regulates the development of some organs of Arabidopsis thaliana. The intervention of PDLP5 proteins is decisive for the callose deposition in the PD, which regulates the auxin distribution and impacts root formation, especially at the lateral roots. The participation of TS is important to develop the auxin activity, which favors root formation, necessary for the improvement plant nutrient absorption. This knowledge can be used to improve development plants of agronomic interest.
References
Amsbury, S., Kirk, P., and Benítez-Alfonso, Y. (2018). Emerging models on the regulation of intracellular transport by plasmodesmata-associated callose. Journal of Experimental Botany. 69(1): 105-115. DOI: https://doi.org/10.1093/jxb/erx337
Band, R. L. (2021). Auxin fluxes through plasmodesmata. New Phytologist. 231(5): 1686-1692. DOI: https://doi.org/10.1111/nph.17517
Barr, Z. and Tilsne, J. (2023). Cell-to-cell connectivity assays for the analysis of cytoskeletal and other regulators of plasmodesmata. Methods in Molecular Biology. 2604: 193-202. DOI: https://doi.org/10.1007/978-1-0716-2867-6_14
Benitez-Alfonso, Y., Faulkner, C., Pendle, A., Miyashima, S., Helariuta, Y., and Maule, A. (2013). Symplastic intercellular connectivity regulates lateral root patterning. Development Cell. 26(2): 136-147. DOI: https://doi.org/10.1016/j.devcel.2013.06.010
Brunkard, J. O. (2020). Exaptive evolution of target of rapamycin signaling in multicellular eukaryotes. Development Cell. 54(2): 142-155. DOI: https://doi.org/10.1016/j.devcel.2020.06.022
Cao, X., Yang, H., Shang, C., Sang, M., Liu, L., and Cheng, J. (2019). The roles of auxin biosynthesis YUCCA gene family in plants. International Journal of Molecular Science. 20(24): 6343. DOI: https://doi.org/10.3390/ijms20246343
Chang, W., Guo, Y., Zhang, H., Liu, X., and Guo, L. (2020). Same actor in different stages: Genes in shoot apical meristem maintenance and floral meristem determinacy in Arabidopsis. Frontiers in Ecology and Evolution. 8: 89. DOI: https://doi.org/10.3389/fevo.2020.00089
Chen, X. Y., Liu, L., Lee, E., Han, X., Rim, Y., Chu, H., and Kim, J. Y. (2009). The Arabidopsis callose synthase gene GSL8 is required for cytokinesis and cell patterning. Plant Physiology. 150(1): 105-113. DOI: https://doi.org/10.1104/pp.108.133918
Faulkner, C. (2018). Plasmodesmata and the symplast. Current Biology. 28(24): R1374-R1378. DOI: https://doi.org/10.1016/j.cub.2018.11.004
Finet, C. and Jaillais, Y. (2012). AUXOLOGY: When auxin meets plant evo devo. Developmental Biology. 365(1): 19-31. DOI: https://doi.org/10.1016/j.ydbio.2012.05.039
Fuchs, M. and Lohmann, J. U. (2020). Aiming for the top: non-cell autonomous control of shoot stem cell in Arabidopsis. Journal Plant Research. 133: 297-309. DOI: https://doi.org/10.1007/s10265-020-01174-3
Gaillochet, C. and Lohmann, J. U. (2015). The never-ending story: from pluripotency to plant developmental plasticity. Development. 142(13): 2237-2249. DOI: https://doi.org/10.1242/dev.117614
Gao, C., Liu, X., De-Storme, N., Jensen, K. H., Xu, Q., Yang, J., …, and Liesche, J. (2020). Directionality of plasmodesmata-mediated transport in Arabidopsis leaves support auxin channeling. Current Biology. 30(10): 1970-1977. DOI: https://doi.org/10.1016/j.cub.2020.03.014
García-Gómez, M. L., Garay-Arroyo, A., García-Ponce, B., Paz-Sánchez, M., and Álvarez-Buylla, E. R. (2021). Hormonal regulation of stem cell proliferation at the Arabidopsis thaliana root stem cell niche. Frontiers in Plant Science. 12: 628491. DOI: https://doi.org/10.3389/fpls.2021.628491
Habets, M. E. J. and Offringa, R. (2014). PIN-driven polar auxin transport in plant developmental plasticity: a key target for environmental and endogenous signals. New Phytologist. 203(2): 362-377. DOI: https://doi.org/10.1111/nph.12831
Han, H., Adamowski, M., Qi, L., Alotaibi, S. S., and Friml, J. (2021). PIN-mediated polar auxin transport regulations in plant tropic response. New Phytologist. 232: 510-522. DOI: https://doi.org/10.1111/nph.17617
Han, X., Hyun, T. K., Zhang, M., Kumar, R., Koh, E. J., Kang, B. H., and Kim, J. Y. (2014). Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Developmental Cell. 28(2): 132-146. DOI: https://doi.org/10.1016/j.devcel.2013.12.008
Hernández-Hernández, V., Benítez, M., and Boudaoud, A. (2020). Interplay between turgor pressure and plasmodesmata during plant development. Journal of Experimental Botany. 71(3): 768-777. DOI: https://doi.org/10.1093/jxb/erz434
Hussain, S., Nanda, S., Zhang, J., Rehmani, M. I. A., Suleman, M., Li, G., and Hou, H. (2021). Auxin and cytokinin interplay during leaf morphogenesis and phyllotaxy. Plants. 10(8): 1732. DOI: https://doi.org/10.3390/plants10081732
Jiang, Y., Zheng, W., Li, J., Lui, P., Zhong, K., Jin, P., …, and Chen, J. (2021). NbWRKY40 positively regulates the response of Nicotiana benthamiana to tomato mosaic virus via salicylic acid signaling. Frontiers in Plant Science. 11: 603518. DOI: https://doi.org/10.3389/fpls.2020.603518
Kumar, N. and Iyer-Pascuzzi, A. S. (2020). Shedding the last layer: Mechanisms of root cap cell release. Plants. 9(3): 308. DOI: https://doi.org/10.3390/plants9030308
Lee, H., Ganguly, A., Lee, R. D., Park, M., and Cho, H. T. (2020). Intracellular localized PIN-FORMED8 promotes lateral root emergence in Arabidopsis. Frontiers in Plant Science. 10: 1808. DOI: https://doi.org/10.3389/fpls.2019.01808
Leyser, O. (2018). Auxin signaling. Plant Physiology. 176(1): 465-479. DOI: https://doi.org/10.1104/pp.17.00765
Li, N., Lin, Z., Yu, P., Zeng, Y., Du, S., and Huang, L. J. (2023). The multifarious role of callose and callose synthase in plants development and environment interactions. Frontiers in Plant Science. 14: 1183402. DOI: https://doi.org/10.3389/fpls.2023.1183402
Li, R., Wei, Z., Li, Y., Shang, X., Cao, Y., Duan, L., …, and Ma., L. (2022a). Ski-interacting protein interacts with shoot meristem less to regulate shoot apical meristem formation. Plant Physiology. 189(4): 2193-2209. DOI: https://doi.org/10.1093/plphys/kiac241
Li, Z., Liu, S. L., Montes-Serey, C., Walley, J. W., and Aung, K. (2022b). Plasmodesmata-located proteins regulate plasmodesmal function at specific cell interface in Arabidopsis. BioRxiv. 08.05.50299. DOI: https://doi.org/10.1101/2022.08.05.502996
Liu, J., Zhang, L., and Yan, D. (2021). Plasmodes-matainvolved battle against pathogens and potential strategies for strengthening hosts. Frontiers in Plant Science. 12: 644870. DOI: https://doi.org/10.3389/fpls.2021.644870
Malamy, J. E. and Benfey, P. N. (1997). Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development. 124(1): 33-44. DOI: https://doi.org/10.1242/dev.124.1.33
Mellor, N. L., Voß, U., Janes, G., Bennett, M. J., Wells, D. M., and Band, L. R. (2020). Auxin fluxes through plasmodesmata modify root-tip auxin distribution. Development. 147(6): dev181669. DOI: https://doi.org/10.1242/dev.181669
Michniewicz, M., Brewer, P. B., and Friml, J. (2007). Polar auxin transport and asymmetric auxin distribution. The Arabidopsis Book/American Society of Plant Biologists. 5: e0108.
Mishra, B. S., Sharma, M., and Laxmi, A. (2022). Role of sugar and auxin crosstalk in plant growth and development. Physiologia Plantarum. 174(1): e13546. DOI: https://doi.org/10.1111/ppl.13546
Nie, P., Li, X., Wang, S., Guo, J., Zhao, H., and Niu, D. (2017). Induced system resistance against Botrytis cinerea by Bacillus cereus AR156 through a JA/ET-and NPR1-dependent signaling pathway and activates PAMP-triggers immunity in Arabidopsis. Frontiers in Plant Science. 8: 238. DOI: https://doi.org/10.3389/fpls.2017.00238
Nishikawa, S., Zinkl, G. M., Swanson, R. J., Maruyama, D., and Preuss, D. (2005). Callose (beta-1 3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biology. 5(1): 1-9. DOI: https://doi.org/10.1186/1471-2229-5-22
Ötvos, K., Marconi, A., Vega, A., O´Brien, J., Johnson, A., Abualia, R., and Benková, E. (2019). Modulation of plant root growth by nitrogen source-defined regulation of polar auxin transport. The EMBO Journal. 40(3): e106862. DOI: https://doi.org/10.15252/embj.2020106862
Peris, L. C. I., Rademacher, E. H., and Weijers, D. (2010). Green beginnings-pattern formation in the early plant embryo. Current Topics in Developmental Biology. 91: 1-27. DOI: https://doi.org/10.1016/S0070-2153(10)91001-6
Peters, W. S., Jensen, K. H., Stone, H. A., and Knoblauch, K. (2021). Plasmodesmata and the problems with size: Interpreting the confusion. Journal of Plant Physiology. 257: 153341. DOI: https://doi.org/10.1016/j.jplph.2020.153341
Robert, H. S. and Friml, J. (2009). Auxin and other signal on the move in plants. Nature Chemical Biology. 5: 325-332. DOI: https://doi.org/10.1038/nchembio.170
Rosquete, M. R., Barbez, E., and Kleine-Vehn, J. (2012). Cellular auxin homeostasis: gatekeeping in housekeeping. Molecular Plant. 5(4): 772-786. DOI: https://doi.org/10.1093/mp/ssr109
Rutschow, H. L., Baskin, T. I., and Kramer, E. M. (2011). Regulation of solute flux through plasmodes mata in the root meristem. Plant Physiology. 155(4): 1817-1826. DOI: https://doi.org/10.1104/pp.110.168187
Sager, R., Bennett, M., and Lee, J. Y. (2021). A tale of two domains pushing lateral roots. Trends in Plant Science. 26(8): 770-779. DOI: https://doi.org/10.1016/j.tplants.2021.01.006
Sager, R., Wang, X., Hill, K., Yoo, B. C., Caplan, J., Nedo, A., and Lee, J. Y. (2020). Auxindependent control of a plasmodesmal regulator creates a negative feedback loop modulating lateral root emergence. Nature Communications. 11(1): 364. DOI: https://doi.org/10.1038/s41467-019-14226-7
Sauer, M. and Kleine-Vehn, J. (2019). PIN-FORMED and PIN-LIKES auxin transport facilitators. Development. 146(15): dev168088. DOI: https://doi.org/10.1242/dev.168088
Scarpella, E., Barkoulas, M., and Tsiantis, M. (2010). Control of leaf and vein development by auxin. Cold Spring Harbor Perspectives in Biology. 2(1): a001511. DOI: https://doi.org/10.1101/cshperspect.a001511
Schaller, G. E., Bishopp, A., and Kieber, J. J. (2015).
The Yin-Yang of hormones: cytokinin and auxin interactions in plant development. The Plant Cell. 27(1): 44-63. DOI: https://doi.org/10.1105/tpc.114.133595
Scheres, B. (2007). Stem-cell niches: nursery rhymes across kingdoms. Nature Reviews Molecular Cell Biology. 8(5): 345-354. DOI: https://doi.org/10.1038/nrm2164
Simpson, C., Thomas, C., Findlay, K., Bayer, E., and Maule, A. J. (2009). An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell to-cell trafficking. The Plant Cell. 21(2): 581-594. DOI: https://doi.org/10.1105/tpc.108.060145
Strotmann, A. I. and Stahl, Y. (2021). At the root of quiescence: function and regulation of the quiescent center. Journal of Experimental Botany. 72(19): 6716-6726. DOI: https://doi.org/10.1093/jxb/erab275
Taiz, L. and Zeiger, E. (2010). Auxin: The first discovered plant growth hormone. In L. Taiz, L. and E. Zeiger (Eds.), Plant Physiology, (Fifth edition). (pp. 545-582). Massachusetts U.S.A. Sinauer Associates Inc, Publishers.
Tee, E. E., Johnston, M. G., Papp, D., and Faulkner, C. (2023). A PDLP-NHL3 complex integrates plasmodesmal immune signaling cascades. Proceedings of the National Academy of Sciences. 120(17): e2216397120. DOI: https://doi.org/10.1073/pnas.2216397120
Thomas, C. L., Mayer, E. M., Ritzenthaler, C., Fernandez-Calvino, L., and Maule, A. J. (2008). Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biology. 6(1): e7. DOI: https://doi.org/10.1371/journal.pbio.0060007
Torres-Martínez, H. G., Rodríguez-Alonso, G., Shishkova, S., and Dubrovsky, J. G. (2019). Lateral root primordium morphogenesis in angiosperms. Frontiers in Plant Science. 10: 206. DOI: https://doi.org/10.3389/fpls.2019.00206
Tylewicz, S., Petterle, A., Marttila, S., Miskolczi, P., Azeez, A., and Bhalerao, R. P. (2018). Photoperiodic control of seasonal growth is mediated by ABA ac-tion on cell-cell communication. Science. 350(6385): 212-215. DOI: https://doi.org/10.1126/science.aan8576
Uchida, N. and Torii, K. U. (2019). Stem cells within the shoot apical meristem: identity, arrangement and communication. Cellular and Molecular Life Sciences. 76(6): 1067-1080. DOI: https://doi.org/10.1007/s00018-018-2980-z
Vatén, A., Dettmer, J., Wu, S., Stierhor, Y. D., Miyashima, S., Yadav, S. R., …, and Helariutta, Y. (2011). Callose biosynthesis regulates symplastic trafficking during root development. Developmental Cell. 21(6): 1144-1155. DOI: https://doi.org/10.1016/j.devcel.2011.10.006
Vázquez-Chimalhua, E., López-Bucio, J., Valencia- Cantero, E. y Beltrán-Peña, E. (2018). Mecanismos moleculares que controlan el desarrollo de los meristemos en plantas. En E. Beltrán-Peña, J. López-Bucio y M. Martínez-Trujillo (Eds.), Fronteras en la biología: Señalización y comunicación de las plantas (pp. 28-39). Morelia: Morevalladolid.
Vicente-Hernández, A., Salgado-Garciglia, R., Valencia-Cantero, E., Ramírez-García, A., García-Juárez, P., and Macías-Rodríguez, L. (2019). Bacillus methylotrophicus Ma-96 stimulates the growth of strawberry (Fragaria X ananassa ‘Aromas’) plants in vitro and slows Botrytis cinerea infection by two different methods of interaction. Journal of Plant Growth Regulation. 38(3): 765-777. DOI: https://doi.org/10.1007/s00344-018-9888-6
Wang, A. (2021). Cell-to-cell movement of plant viruses via plasmodesmata: a current perspective on potyviruses. Current Opinion in Virology. 48: 10-16. DOI: https://doi.org/10.1016/j.coviro.2021.03.002
Wang, Y. and Jiao, Y. (2023). Cell signaling in the shoot apical meristem. Plant Physiology. 193(1): 70-82. DOI: https://doi.org/10.1093/plphys/kiad309
Wu, S. W., Kumar, R., Iswanto, A. B. B., and Kim, J. Y. (2018). Callose balancing at plasmodesmata. Journal of Experimental Botany. 69(22): 5325-5339. DOI: https://doi.org/10.1093/jxb/ery317
Zambryski, P. (2004). Cell-to-cell transport of proteins and fluorescent tracers via plasmodesmata during plant development. Journal of Cell Biology. 164(2): 165-168. DOI: https://doi.org/10.1083/jcb.200310048
Zambryski, P. and Crawford, K. (2000). Plasmo-desmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annual Review of Cell and Developmental Biology. 16: 393-421. DOI: https://doi.org/10.1146/annurev.cellbio.16.1.393
Zavaliev, R., Ueki, S., Epel, B. L., and Citovsky, V. (2011). Biology of callose (ß-1,3-glucan) turnover at plasmodesmata. Protoplasma. 248: 117-130. DOI: https://doi.org/10.1007/s00709-010-0247-0
Zažímolová, E., Krecek, P., Skůpa, O., Hoyerová, K., and Patrásek, J. (2007). Polar transport of the plant hormone auxin- the role of PIN-FORMED (PIN) proteins. Cellular and Molecular Life Sciences. 64(13): 1621-1637. DOI: https://doi.org/10.1007/s00018-007-6566-4
Zhang, J. and Peer, W. A. (2017). Auxin homeostasis: the DAO of catabolism. Journal of Experimental Botany. 68(12): 3145-3154. DOI: https://doi.org/10.1093/jxb/erx221
Zhang, Y., Yu. J., Xu, X., Wang, R., Liu, Y., Huang, S., …, and Wei, Z. (2022). Molecular mechanisms of diverse auxin responses during plant growth and development. International Journal of Molecular Science. 23(20): 12495. DOI: https://doi.org/10.3390/ijms232012495
Published
How to Cite
License
Copyright (c) 2023 Universidad Autónoma de Tamaulipas
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Accepted 2024-01-24
Published 2024-01-30
