The role of indole-3-acetic acid and characterization of PIN transporters in complex streptophyte alga Chara braunii
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
I 6123-B
Austrian Science Fund
20-13587S
Grantová Agentura České Republiky
289523
Grantová Agentura, Univerzita Karlova
393422
Grantová Agentura, Univerzita Karlova
PubMed
40047465
PubMed Central
PMC11982790
DOI
10.1111/nph.70019
Knihovny.cz E-zdroje
- Klíčová slova
- Chara, auxin transport, indole‐3‐acetic acid, plant evolution, streptophytes,
- MeSH
- biologický transport účinky léků MeSH
- buněčná membrána metabolismus účinky léků MeSH
- Chara * metabolismus účinky léků MeSH
- fosforylace účinky léků MeSH
- kyseliny indoloctové * metabolismus farmakologie MeSH
- membránové transportní proteiny * metabolismus MeSH
- rostlinné proteiny * metabolismus MeSH
- tabák metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- indoleacetic acid MeSH Prohlížeč
- kyseliny indoloctové * MeSH
- membránové transportní proteiny * MeSH
- rostlinné proteiny * MeSH
Auxin, indole-3-acetic acid (IAA), is a key phytohormone with diverse morphogenic roles in land plants, but its function and transport mechanisms in algae remain poorly understood. We therefore aimed to explore the role of IAA in a complex, streptophyte algae Chara braunii. Here, we described novel responses of C. braunii to IAA and characterized two homologs of PIN auxin efflux carriers: CbPINa and CbPINc. We determined their localization in C. braunii using epitope-specific antibodies and tested their function in heterologous land plant models. Further, using phosphoproteomic analysis, we identified IAA-induced phosphorylation events. The thallus regeneration assay showed that IAA promotes thallus elongation and side branch development. Immunolocalization of CbPINa and CbPINc confirmed their presence on the plasma membrane of vegetative and generative cells of C. braunii. However, functional assays in tobacco BY-2 cells demonstrated that CbPINa affects auxin transport, whereas CbPINc does not. The IAA is effective in the acceleration of cytoplasmic streaming and the phosphorylation of evolutionary conserved targets such as homolog of RAF-like kinase. These findings suggest that, although canonical PIN-mediated auxin transport mechanisms might not be fully conserved in Chara, IAA is involved in morphogenesis and fast signaling processes.
Faculty of Biotechnology University of Wroclaw Joliot Curie 14a Wroclaw 50 383 Poland
Institute of Science and Technology Austria Klosterneuburg 3400 Austria
Laboratory of Biochemistry Wageningen University Stippeneng 4 Wageningen 6708 SP the Netherlands
School of Biological Sciences Monash University Melbourne 3800 Vic Australia
Zobrazit více v PubMed
Abas L, Kolb M, Stadlmann J, Janacek DP, Lukic K, Schwechheimer C, Sazanov LA, Mach L, Friml J, Hammes UZ. 2021. Naphthylphthalamic acid associates with and inhibits PIN auxin transporters. Proceedings of the National Academy of Sciences, USA 118: e2020857118. PubMed PMC
Abraham MJ, Murtola T, Schulz R, Páll S, Smith JC, Hess B, Lindahl E. 2015. GROMACS: High performance molecular simulations through multi‐level parallelism from laptops to supercomputers. SoftwareX 1–2: 19–25.
An G. 1985. High efficiency transformation of cultured tobacco cells 1. Plant Physiology 79: 568–570. PubMed PMC
Barbier FF, Dun EA, Kerr SC, Chabikwa TG, Beveridge CA. 2019. An update on the signals controlling shoot branching. Trends in Plant Science 24: 220–236. PubMed
Bayly‐Jones C, Lupton CJ, Keen AC, Dong S, Mastos C, Luo W, Qian C, Jones GD, Venugopal H, Chang Y‐G et al. 2024. LYCHOS is a human hybrid of a plant‐like PIN transporter and a GPCR. Nature 634: 1238–1244. PubMed PMC
Becker B, Marin B. 2009. Streptophyte algae and the origin of embryophytes. Annals of Botany 103: 999–1004. PubMed PMC
Beilby MJ, Turi CE, Baker TC, Tymm FJ, Murch SJ. 2015. Circadian changes in endogenous concentrations of indole‐3‐acetic acid, melatonin, serotonin, abscisic acid and jasmonic acid in Characeae (Chara australis Brown). Plant Signaling & Behavior 10: e1082697. PubMed PMC
Bennett T, Brockington SF, Rothfels C, Graham SW, Stevenson D, Kutchan T, Rolf M, Thomas P, Wong GK‐S, Leyser O et al. 2014. Paralogous radiations of PIN proteins with multiple origins of noncanonical PIN structure. Molecular Biology and Evolution 31: 2042–2060. PubMed PMC
Best RB, Zhu X, Shim J, Lopes PEM, Mittal J, Feig M, MacKerell AD. 2012. Optimization of the additive CHARMM all‐atom protein force field targeting improved sampling of the backbone φ, ψ and side‐chain χ1 and χ2 dihedral angles. Journal of Chemical Theory and Computation 8: 3257–3273. PubMed PMC
Bierenbroodspot MJ, Pröschold T, Fürst‐Jansen JMR, de Vries S, Irisarri I, Darienko T, de Vries J. 2024. Phylogeny and evolution of streptophyte algae. Annals of Botany 134: 385–400. PubMed PMC
Blake TJ, Reid DM, Rood SB. 1983. Ethylene, indoleacetic acid and apical dominance in peas: a reappraisal. Physiologia Plantarum 59: 481–487.
Boot KJM, Libbenga KR, Hille SC, Offringa R, van Duijn B. 2012. Polar auxin transport: an early invention. Journal of Experimental Botany 63: 4213–4218. PubMed PMC
Bowman JL. 2022. The origin of a land flora. Nature Plants 8: 1352–1369. PubMed
Bowman JL, Flores Sandoval E, Kato H. 2021. On the evolutionary origins of land plant auxin biology. Cold Spring Harbor Perspectives in Biology 13: a040048. PubMed PMC
Bulychev AA, Cherkashin AA, Rubin AB, Vredenberg WJ, Zykov VS, Müller SC. 2001. Comparative study on photosynthetic activity of chloroplasts in acid and alkaline zones of Chara corallina . Bioelectrochemistry 53: 225–232. PubMed
Buschmann H. 2020. Into another dimension: how streptophyte algae gained morphological complexity. Journal of Experimental Botany 71: 3279–3286. PubMed
Carrillo‐Carrasco VP, Hernandez‐Garcia J, Mutte SK, Weijers D. 2023. The birth of a giant: evolutionary insights into the origin of auxin responses in plants. EMBO Journal 42: e113018. PubMed PMC
Causse HB. 1993. Marchantia L: the European and African Taxa. Berlin, Germany: J Cramer.
Chau R, Bisson MA, Siegel A, Elkin G, Klim P, Straubinger RM. 1994. Distribution of charasomes in chara: re‐establishment and loss in darkness and correlation with banding and inorganic carbon uptake. Functional Plant Biology 21: 113–123.
Cheng S, Xian W, Fu Y, Marin B, Keller J, Wu T, Sun W, Li X, Xu Y, Zhang Y et al. 2019. Genomes of subaerial zygnematophyceae provide insights into land plant evolution. Cell 179: 1057–1067. PubMed
Clabeaux BL, Navarro DAG, Aga DS, Bisson MA. 2011. Cd tolerance and accumulation in the aquatic macrophyte, Chara australis: potential use for charophytes in phytoremediation. Environmental Science & Technology 45: 5332–5338. PubMed
Delbarre A, Muller P, Imhoff V, Guern J. 1996. Comparison of mechanisms controlling uptake and accumulation of 2,4‐dichlorophenoxy acetic acid, naphthalene‐1‐acetic acid, and indole‐3‐acetic acid in suspension‐cultured tobacco cells. Planta 198: 532–541. PubMed
Dibb‐Fuller JE, Morris DA. 1992. Studies on the evolution of auxin carriers and phytotropin receptors: transmembrane auxin transport in unicellular and multicellular Chlorophyta. Planta 186: 219–226. PubMed
Donoghue PCJ, Harrison CJ, Paps J, Schneider H. 2021. The evolutionary emergence of land plants. Current Biology 31: R1281–R1298. PubMed
Edgar RC. 2004. muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797. PubMed PMC
Feng X, Zheng J, Irisarri I, Yu H, Zheng B, Ali Z, de Vries S, Keller J, Fürst‐Jansen JMR, Dadras A et al. 2024. Genomes of multicellular algal sisters to land plants illuminate signaling network evolution. Nature Genetics 56: 1018–1031. PubMed PMC
Fisher TJ, Flores‐Sandoval E, Alvarez JP, Bowman JL. 2023. PIN‐FORMED is required for shoot phototropism/gravitropism and facilitates meristem formation in Marchantia polymorpha. New Phytologist 238: 1498–1515. PubMed
Flores‐Sandoval E, Eklund DM, Bowman JL. 2015. A simple auxin transcriptional response system regulates multiple morphogenetic processes in the liverwort marchantia polymorpha. PLoS Genetics 11: e1005207. PubMed PMC
Foissner I, Sommer A, Hoeftberger M. 2015. Photosynthesis‐dependent formation of convoluted plasma membrane domains in Chara internodal cells is independent of chloroplast position. Protoplasma 252: 1085–1096. PubMed PMC
Friml J. 2022. Fourteen stations of auxin. Cold Spring Harbor Perspectives in Biology 14: a039859. PubMed PMC
Friml J, Gallei M, Gelová Z, Johnson A, Mazur E, Monzer A, Rodriguez L, Roosjen M, Verstraeten I, Živanović BD et al. 2022. ABP1‐TMK auxin perception for global phosphorylation and auxin canalization. Nature 609: 575–581. PubMed
Gamborg OL, Miller RA, Ojima K. 1968. Nutrient requirements of suspension cultures of soybean root cells. Experimental Cell Research 50: 151–158. PubMed
Gao X, Nagawa S, Wang G, Yang Z. 2008. Cell polarity signaling: focus on polar auxin transport. Molecular Plant 1: 899–909. PubMed PMC
Goddard TD, Huang CC, Meng EC, Pettersen EF, Couch GS, Morris JH, Ferrin TE. 2018. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Science 27: 14–25. PubMed PMC
Godlewski M. 1980. Auxin as a factor regulating initiation, of mitosis in antheridial filaments of Chara vulgaris L. Biochemie und Physiologie der Pflanzen 175: 314–321.
Hackenberg D, Pandey S. 2014. Heterotrimeric G‐proteins in green algae: an early innovation in the evolution of the plant lineage. Plant Signaling & Behavior 9: e28457. PubMed PMC
Harrison J. 2017. Development and genetics in the evolution of land plant body plans. Philosophical Transactions of the Royal Society, B: Biological Sciences 372: 20150490. PubMed PMC
Hernández‐García J, Carrillo‐Carrasco VP, Rienstra J, Tanaka K, De RM, Dipp‐Álvarez M, Freire‐Ríos A, Crespo I, Boer DR, van Den BWAM et al. 2024. Evolutionary origins and functional diversification of auxin response factors. Nature Communications 15: 10909. PubMed PMC
Heß D, Heise CM, Schubert H, Hess WR, Hagemann M. 2023a. The impact of salt stress on the physiology and the transcriptome of the model streptophyte green alga Chara braunii . Physiologia Plantarum 175: e14123. PubMed
Heß D, Holzhausen A, Hess WR. 2023b. Insight into the nodal cells transcriptome of the streptophyte green alga Chara braunii S276. Physiologia Plantarum 175: e14025. PubMed
Holzhausen A, Stingl N, Rieth S, Kühn C, Schubert H, Rensing SA. 2022. Establishment and optimization of a new model organism to study early land plant evolution: germination, cultivation and oospore variation of Chara braunii Gmelin, 1826. Frontiers in Plant Science 13: 987741. PubMed PMC
Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, Sato S, Yamada T, Mori H, Tajima N et al. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications 5: 3978. PubMed PMC
Ishizaki K, Chiyoda S, Yamato KT, Kohchi T. 2008. Agrobacterium‐mediated transformation of the haploid liverwort Marchantia polymorpha L., an emerging model for plant biology. Plant and Cell Physiology 49: 1084–1091. PubMed
Ishizaki K, Nishihama R, Ueda M, Inoue K, Ishida S, Nishimura Y, Shikanai T, Kohchi T. 2015. Development of gateway binary vector series with four different selection markers for the liverwort marchantia polymorpha. PLoS ONE 10: e0138876. PubMed PMC
Jahnke E, Libbert E. 1964. Indol‐3‐essigsäure Als Einziges Natives Auxin Bei Chara‐Arten. Plant Signaling & Behavior 52: 283–290.
Janacek DP, Kolb M, Schulz L, Mergner J, Kuster B, Glanc M, Friml J, Tusscher K, Schwechheimer C, Hammes UZ. 2024. Transport properties of canonical PIN‐FORMED proteins from Arabidopsis and the role of the loop domain in auxin transport. Developmental Cell 59: 3259–3271. PubMed
Jin Q, Scherp P, Heimann K, Hasenstein KH. 2008. Auxin and cytoskeletal organization in algae. Cell Biology International 32: 542–545. PubMed
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A et al. 2021. Highly accurate protein structure prediction with alphafold . Nature 596: 583–589. PubMed PMC
Klämbt D, Knauth B, Dittmann I. 1992. Auxin dependent growth of rhizoids of Chara globularis . Physiologia Plantarum 85: 537–540.
Kuhn A, Roosjen M, Mutte S, Dubey SM, Carrillo Carrasco VP, Boeren S, Monzer A, Koehorst J, Kohchi T, Nishihama R et al. 2024. RAF‐like protein kinases mediate a deeply conserved, rapid auxin response. Cell 187: 130–148. PubMed PMC
Kurtović K, Schmidt V, Nehasilová M, Vosolsobě S, Petrášek J. 2024. Rediscovering Chara as a model organism for molecular and evo‐devo studies. Protoplasma 261: 183–196. PubMed
Laskowski RA, Swindells MB. 2011. LigPlot+: multiple ligand–protein interaction diagrams for drug discovery. Journal of Chemical Information and Modeling 51: 2778–2786. PubMed
Liang Z, Geng Y, Ji C, Du H, Wong CE, Zhang Q, Zhang Y, Zhang P, Riaz A, Chachar S et al. 2020. Mesostigma viride genome and transcriptome provide insights into the origin and evolution of streptophyta. Advanced Science 7: 1901850. PubMed PMC
Luschnig C, Friml J. 2024. Over 25 years of decrypting PIN‐mediated plant development. Nature Communications 15: 9904. PubMed PMC
Lv S, Wang L, Zhang X, Li X, Fan L, Xu Y, Zhao Y, Xie H, Sawchuk M, Scarpella E et al. 2020. Arabidopsis NHX5 and NHX6 regulate PIN6‐mediated auxin homeostasis and growth. Journal of Plant Physiology 255: 153305. PubMed
Métraux JP, Richmond PA, Taiz L. 1980. Control of cell elongation in nitella by endogenous cell wall pH gradients: MULTIAXIAL EXTENSIBILITY AND GROWTH STUDIES 1. Plant Physiology 65: 204–210. PubMed PMC
Mirdita M, Schütze K, Moriwaki Y, Heo L, Ovchinnikov S, Steinegger M. 2022. colabfold: making protein folding accessible to all. Nature Methods 19: 679–682. PubMed PMC
Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A, Petrášek J, Zhang J, Gaykova V, Stierhof Y‐D et al. 2009. Subcellular homeostasis of phytohormone auxin is mediated by the ER‐localized PIN5 transporter. Nature 459: 1136–1140. PubMed
Müller K, Hošek P, Laňková M, Vosolsobě S, Malínská K, Čarná M, Fílová M, Dobrev PI, Helusová M, Hoyerová K et al. 2019. Transcription of specific auxin efflux and influx carriers drives auxin homeostasis in tobacco cells. The Plant Journal 100: 627–640. PubMed
Murashige T, Skoog F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15: 473–497.
Mutte SK, Kato H, Rothfels C, Melkonian M, Wong GK‐S, Weijers D. 2018. Origin and evolution of the nuclear auxin response system. eLife 7: e33399. PubMed PMC
Naramoto S. 2017. Polar transport in plants mediated by membrane transporters: focus on mechanisms of polar auxin transport. Current Opinion in Plant Biology 40: 8–14. PubMed
Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint‐Marcoux D, Ullrich KK, Haas FB, Vanderstraeten L, Becker D, Lang D et al. 2018. The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174: 448–464. PubMed
Pan L, Fonseca De Lima CF, Vu LD, De Smet I. 2021. A comprehensive phylogenetic analysis of the MAP4K family in the green lineage. Frontiers in Plant Science 12: 2541. PubMed PMC
Petrášek J, Černá A, Schwarzerová K, Elčkner M, Morris DA, Zažímalová E. 2003. Do phytotropins inhibit auxin efflux by impairing vesicle traffic? Plant Physiology 131: 254–263. PubMed PMC
Petrášek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D, Wiśniewska J, Tadele Z, Kubeš M, Čovanová M et al. 2006. PIN proteins perform a rate‐limiting function in cellular auxin efflux. Science 312: 914–918. PubMed
Pollak B, Cerda A, Delmans M, Álamos S, Moyano T, West A, Gutiérrez RA, Patron NJ, Federici F, Haseloff J. 2019. Loop assembly: a simple and open system for recursive fabrication of DNA circuits. New Phytologist 222: 628–640. PubMed
Ravindranath PA, Forli S, Goodsell DS, Olson AJ, Sanner MF. 2015. AutoDockFR: advances in protein‐ligand docking with explicitly specified binding site flexibility. PLoS Computational Biology 11: e1004586. PubMed PMC
Sauer M, Kleine‐Vehn J. 2019. PIN‐FORMED and PIN‐LIKES auxin transport facilitators. Development 146: dev168088. PubMed
Schmidt V, Skokan R, Depaepe T, Kurtović K, Haluška S, Vosolsobě S, Vaculíková R, Pil A, Dobrev PI, Motyka V et al. 2024. Phytohormone profiling in an evolutionary framework. Nature Communications 15: 3875. PubMed PMC
Schmölzer PM, Höftberger M, Foissner I. 2011. Plasma membrane domains participate in pH banding of Chara internodal cells. Plant & Cell Physiology 52: 1274–1288. PubMed PMC
Skokan R, Medvecká E, Viaene T, Vosolsobě S, Zwiewka M, Müller K, Skůpa P, Karady M, Zhang Y, Janacek DP et al. 2019. PIN‐driven auxin transport emerged early in streptophyte evolution. Nature Plants 5: 1114–1119. PubMed
Su N, Zhu A, Tao X, Ding ZJ, Chang S, Ye F, Zhang Y, Zhao C, Chen Q, Wang J et al. 2022. Structures and mechanisms of the Arabidopsis auxin transporter PIN3. Nature 609: 616–621. PubMed
Sztein AE, Cohen JD, Cooke TJ. 2000. Evolutionary patterns in the auxin metabolism of green plants. International Journal of Plant Sciences 161: 849–859.
Takahashi K, Hayashi K, Kinoshita T. 2012. Auxin activates the plasma membrane H+‐ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiology 159: 632–641. PubMed PMC
Tyanova S, Temu T, Cox J. 2016a. The MaxQuant computational platform for mass spectrometry‐based shotgun proteomics. Nature Protocols 11: 2301–2319. PubMed
Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J. 2016b. The Perseus computational platform for cosmprehensive analysis of (prote)omics data. Nature Methods 13: 731–740. PubMed
Ung KL, Schulz L, Stokes DL, Hammes UZ, Pedersen BP. 2023. Substrate recognition and transport mechanism of the PIN‐FORMED auxin exporters. Trends in Biochemical Sciences 48: 937–948. PubMed PMC
Ung KL, Winkler M, Schulz L, Kolb M, Janacek DP, Dedic E, Stokes DL, Hammes UZ, Pedersen BP. 2022. Structures and mechanism of the plant PIN‐FORMED auxin transporter. Nature 609: 605–610. PubMed PMC
Vieten A, Vanneste S, Wiśniewska J, Benková E, Benjamins R, Beeckman T, Luschnig C, Friml J. 2005. Functional redundancy of PIN proteins is accompanied by auxin‐dependent cross‐regulation of PIN expression. Development 132: 4521–4531. PubMed
Vosolsobě S, Petrášek J, Schwarzerová K. 2017. Evolutionary plasticity of plasma membrane interaction in DREPP family proteins. Biochimica et Biophysica Acta (BBA) ‐ Biomembranes 1859: 686–697. PubMed
Vosolsobě S, Skokan R, Petrášek J. 2020. The evolutionary origins of auxin transport: what we know and what we need to know. Journal of Experimental Botany 71: 3287–3295. PubMed
Wasteneys GO, Jablonsky PP, Williamson RE. 1989. Assembly of purified brain tubulin at cortical and endoplasmic sites in perfused internodal cells of the alga Nitella tasmanica . Cell Biology International Reports 13: 513–528.
Weller B, Zourelidou M, Frank L, Barbosa ICR, Fastner A, Richter S, Jürgens G, Hammes UZ, Schwechheimer C. 2017. Dynamic PIN‐FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux‐dependent growth. Proceedings of the National Academy of Sciences, USA 114: E887–E896. PubMed PMC
Wiśniewska J, Xu J, Seifertová D, Brewer PB, Růžička K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J. 2006. Polar PIN localization directs auxin flow in plants. Science 312: 883. PubMed
Yang Z, Xia J, Hong J, Zhang C, Wei H, Ying W, Sun C, Sun L, Mao Y, Gao Y et al. 2022. Structural insights into auxin recognition and efflux by Arabidopsis PIN1. Nature 609: 611–615. PubMed PMC
Żabka A, Polit JT, Winnicki K, Paciorek P, Juszczak J, Nowak M, Maszewski J. 2016. PIN2‐like proteins may contribute to the regulation of morphogenetic processes during spermatogenesis in Chara vulgaris . Plant Cell Reports 35: 1655–1669. PubMed PMC
Zeng HY, Deng S, Jin C, Shang Z, Chang L, Wang J, Han X, Wang A, Jin D, Wang Y et al. 2024. Origin and evolution of auxin‐mediated acid growth. Proceedings of the National Academy of Sciences, USA 121: e2412493121. PubMed PMC
Zhang S, de Boer AH, van Duijn B. 2016. Auxin effects on ion transport in Chara corallina . Journal of Plant Physiology 193: 37–44. PubMed
Zhang Y, Xiao G, Wang X, Zhang X, Friml J. 2019. Evolution of fast root gravitropism in seed plants. Nature Communications 10: 3480. PubMed PMC
Zhao Y, Stoffler D, Sanner M. 2006. Hierarchical and multi‐resolution representation of protein flexibility. Bioinformatics 22: 2768–2774. PubMed
Zuo J, Niu Q‐W, Chua N‐H. 2000. An estrogen receptor‐based transactivator XVE mediates highly inducible gene expression in transgenic plants. The Plant Journal 24: 265–273. PubMed