دورية أكاديمية

ACL5 acquired strict thermospermine synthesis activity during the emergence of vascular plants.

التفاصيل البيبلوغرافية
العنوان: ACL5 acquired strict thermospermine synthesis activity during the emergence of vascular plants.
المؤلفون: Takahashi Y; Department of Life Science, Faculty of Life Science, Kyushu Sangyo University, 2-3-1 Matsukadai Higashi-ku, Fukuoka, 813-8503, Japan.
المصدر: The New phytologist [New Phytol] 2024 Jun; Vol. 242 (6), pp. 2669-2681. Date of Electronic Publication: 2024 Apr 08.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Wiley on behalf of New Phytologist Trust Country of Publication: England NLM ID: 9882884 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1469-8137 (Electronic) Linking ISSN: 0028646X NLM ISO Abbreviation: New Phytol Subsets: MEDLINE
أسماء مطبوعة: Publication: Oxford : Wiley on behalf of New Phytologist Trust
Original Publication: London, New York [etc.] Academic Press.
مواضيع طبية MeSH: Spermine*/metabolism , Spermine*/analogs & derivatives, Substrate Specificity ; Phylogeny ; Nicotiana/genetics ; Nicotiana/metabolism ; Plant Proteins/metabolism ; Plant Proteins/genetics ; Gene Expression Regulation, Plant ; Amino Acid Sequence
مستخلص: Norspermine (Nspm), one of the uncommon polyamines (PAs), was detected in bryophytes and lycophytes; therefore, the aminopropyltransferases involved in the synthesis of Nspm were investigated. The enzymatic activity was evaluated by the transient high expression of various aminopropyltransferase genes in Nicotiana benthamiana, followed by quantification of PA distribution in the leaves using gas chromatography-mass spectrometry. The bryophyte orthologues of ACL5, which is known to synthesise thermospermine (Tspm) in flowering plants, were found to have strong Nspm synthesis activity. In addition, two ACL5 orthologous with different substrate specificities were conserved in Selaginella moellendorffii, one of which was involved in Tspm synthesis and the other in Nspm synthesis. Therefore, further detailed analysis using these two factors revealed that the β-hairpin structural region consisting of β-strands 1 and 2 at the N-terminus of ACL5 is involved in substrate specificity. Through functional analysis of a total of 40 ACL5 genes in 33 organisms, including algae, it was shown that ACL5 has changed its substrate specificity several times during plant evolution and diversification. Furthermore, it was strongly suggested that ACL5 acquired strict Tspm synthesis activity during the emergence of vascular plants, especially through major changes around the β-hairpin structural region.
(© 2024 The Authors New Phytologist © 2024 New Phytologist Foundation.)
References: Alabdallah O, Ahou A, Mancuso N, Pompili V, Macone A, Pashkoulov D, Stano P, Cona A, Angelini R, Tavladoraki P. 2017. The Arabidopsis polyamine oxidase/dehydrogenase 5 interferes with cytokinin and auxin signaling pathways to control xylem differentiation. Journal of Experimental Botany 68: 997–1012.
Baima S, Forte V, Possenti M, Peñalosa A, Leoni G, Salvi S, Felici B, Ruberti I, Morelli G. 2014. Negative feedback regulation of auxin signaling by ATHB8/ACL5‐BUD2 transcription module. Molecular Plant 7: 1006–1025.
Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, de Pamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA et al. 2011. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332: 960–963.
Cai Q, Fukushima H, Yamamoto M, Ishii N, Sakamoto T, Kurata T, Motose H, Takahashi T. 2016. The SAC51 family plays a central role in thermospermine responses in Arabidopsis. Plant and Cell Physiology 57: 1583–1592.
Childs AC, Mehta DJ, Gerner EW. 2003. Polyamine‐dependent gene expression. Cellular and Molecular Life Sciences 60: 1394–1406.
Fuell C, Elliott KA, Hanfrey CC, Franceschetti M, Michael AJ. 2010. Polyamine biocynthetic diversity in plants and algae. Plant Physiology and Biochemistry 48: 513–520.
Gao F, Mei X, Li Y, Guo J, Shen Y. 2021. Update on the roles of polyamines in fleshy fruit ripening, senescence, and quality. Frontiers in Plant Science 12: 610313.
Gerlin L, Baroukh C, Genin S. 2021. Polyamines: double agents in disease and plant immunity. Trends in Plant Science 26: 1061–1071.
Goodin MM, Zaitlin D, Naidu RA, Lommel SA. 2008. Nicotiana benthamiana: its history and future as a model for plant–pathogen interactions. Molecular Plant–Microbe Interactions 21: 1015–1026.
Hamana K, Aizaki T, Saito A, Uchikata K, Ohnishi H. 2004a. Distribution of norspermidine as a cellular polyamine within micro green algae including non‐photosynthetic achlorophyllous Polytoma, Polytomella, Prototheca and Helicosporidium. Journal of General and Applied Microbiology 50: 289–295.
Hamana K, Matsuzaki S. 1985. Distinct difference in the polyamine compositions of Bryophyta and Pteridophyta. Journal of Biochemistry 97: 1595–1601.
Hamana K, Niitsu M. 2006. Cellular polyamines of lower eukaryotes belonging to the phyla Glaucophyta, Rhodophyta, Cryptophyta, Haptophyta and Percolozoa. Journal of General and Applied Microbiology 52: 235–240.
Hamana K, Niitsu M, Hayashi H. 2013. Occurrence of homospermidine and thermospermine as a cellular polyamine in unicellular chlorophyte and multicellular charophyte green algae. Journal of General and Applied Microbiology 59: 313–319.
Hamana K, Sakamoto A, Nishina M, Niitsu M. 2004b. Cellular polyamine profile of the phyla Dinophyta, Apicomplexa, Ciliophora, Euglenozoa, Cercozoa and Heterokonta. Journal of General and Applied Microbiology 50: 297–303.
Hanfrey C, Sommer S, Mayer MJ, Burtin D, Michael AJ. 2001. Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. The Plant Journal 27: 551–560.
Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y. 2000. ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO Journal 19: 4248–4256.
Igarashi K, Kashiwagi K. 2010. Modulation of cellular function by polyamines. The International Journal of Biochemistry and Cell Biology 42: 39–51.
Imai A, Akiyama T, Kato T, Sato S, Tabata S, Yamamoto KT, Takahashi T. 2004a. Spermine is not essential for survival of Arabidopsis. FEBS Letters 556: 148–152.
Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T. 2006. The dwarf phenotype of the Arabidopsis acl5 mutnat is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133: 3575–3585.
Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D et al. 2004b. Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiology 135: 1565–1573.
Kakehi J‐I, Kuwashiro Y, Motose H, Igarashi K, Takahashi T. 2010. Norspermine substitutes for thermospermine in the control of stem elongation in Arabidopsis thaliana. FEBS Letters 584: 3042–3046.
Kakehi J‐I, Kuwashiro Y, Niitsu M, Takahashi T. 2008. Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant and Cell Physiology 49: 1342–1349.
Kamada‐Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M. 2008. A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant and Cell Physiology 49: 1272–1282.
Katayama H, Iwamoto K, Kariya Y, Asakawa T, Kan T, Fukuda H, Ohashi‐Ito K. 2015. A negative feedback loop controlling bHLH complexes is involved in vascular cell division and differentiation in the root apical meristem. Current Biology 25: 3144–3150.
Kim DW, Watanabe K, Murayama C, Izawa S, Niitsu M, Michael AJ, Berberich T, Kusano T. 2014. Polyamine oxidase5 regulates Arabidopsis growth through thermospermine oxidase activity. Plant Physiology 165: 1575–1590.
Knott JM, Römer P, Sumper M. 2007. Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Letters 581: 3081–3086.
Koc EC, Bagga S, Songstad DD, Berz SR, Kuehn GD, Phillips GC. 1998. Occurrence of uncommon polyamines in cultured tissues of maize. In Vitro Cellular & Developmental Biology Plant 34: 252–255.
Kusano T, Berberich T, Tateda C, Takahashi Y. 2008. Polyamines: essential factors for growth and survival. Planta 228: 367–381.
Michael AJ. 2016. Polyamines in eukaryotes, bacteria, and archaea. Journal of Biological Chemistry 291: 14896–14903.
Milhinhos A, Bollhöner B, Blazquez MA, Novák O, Miguel CM, Tuominen H. 2020. ACAULIS5 is required for cytokinin accumulation and function during secondary growth of Populus trees. Frontiers in Plant Science 11: 601858.
Milhinhos A, Prestele J, Bollhöner B, Matos A, Vera‐Sirera F, Rambla JL, Ljung K, Carbonell J, Blázquez MA, Tuominen H et al. 2013. Thermospermine levels are controlled by an auxin‐dependent feedback loop mechanism in Populus xylem. The Plant Journal 75: 685–698.
Minguet EG, Vera‐Sirera F, Marina A, Carbonell J, Blázquez MA. 2008. Evolutionary diversification in polyamine biosynthesis. Molecular Biology and Evolution 25: 2119–2128.
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.
Murashige T, Skoog F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15: 473–497.
Naka Y, Watanabe K, Sagor GHM, Niitsu M, Pillai MA, Kusano T, Takahashi Y. 2010. Quantitative analysis of plant polyamines including thermospermine during growth and salinity stress. Plant Physiology and Biochemistry 48: 527–533.
Panicot M, Minguet EG, Ferrando A, Alcázar R, Blázquez MA, Carbonell J, Altabella T, Koncz C, Tiburcio AF. 2002. A polyamine metabolon involving aminoprophl transferase complexes in Arabidopsis. Plant Cell 14: 2539–2551.
Pegg AE, Michael AJ. 2010. Spermine synthase. Cellular and Molecular Life Sciences 67: 113–121.
Rambla JL, Vera‐Sirera F, Blázquez MA, Carbonell J, Granell A. 2010. Quantitation of biogenic tetraamines in Arabidopsis thaliana. Analytical Biochemistry 397: 208–211.
Rodriguez‐Garay B, Phillips GC, Kuehn GD. 1989. Detection of norspermidine and norspermine in Medicago sativa L. (alfalfa). Plant Physiology 89: 525–529.
Sagor GHM, Inoue M, Kim DW, Kojima S, Niitsu M, Berberich T, Kusano T. 2015. The polyamine oxidase from lycophyte Selaginella lepidophylla (SelPAO5), unlike that of angiosperms, back‐converts thermospermine to norspermidine. FEBS Letters 589: 3701–3708.
Sagor GHM, Kusano T, Berberich T. 2019. A polyamine oxidase from Selaginella lepidophylla (SelPAO5) can replace AtPAO5 in Arabidopsis through converting thermospermine to norspermidine instead to spermidine. Plants 8: 99.
Seiler N, Raul F. 2005. Polyamines and apoptosis. Journal of Cellular and Molecular Medicine 9: 623–642.
Sekula B, Dauter Z. 2018. Crystal structure of thermospermine synthase from Medicago truncatula and substrate discriminatory features of plant aminopropyltransferases. Biochemical Journal 475: 787–802.
Solé‐Gil A, Hernández‐García J, López‐Gresa MP, Blázquez MA, Agustí J. 2019. Conservation of thermospermine synthase activity in vascular and non‐vascular plants. Frontiers in Plant Science 10: 663.
Stecher G, Tamura K, Kumar S. 2020. Molecular evolutionary genetics analysis (MEGA) for macOS. Molecular Biology and Evolution 34: 1237–1239.
Takahashi T, Kakehi J‐I. 2010. Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Annals of Botany 105: 1–6.
Takahashi T, Tong W. 2015. Polyamine catabolism in plants. In: Kusano T, Suzuki H, eds. Polyamines. Tokyo, Japan: Springer, 27–44.
Takahashi Y. 2016. The role of polyamines in plant disease resistance. Environmental Control in Biology 54: 17–21.
Takano A, Kakehi J‐I, Takahashi T. 2012. Thermospermine is not a minor polyamine in the plant kingdom. Plant and Cell Physiology 53: 606–616.
Thompson JD, Higgins DG, Gibson TJ. 1994. ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighing, positions‐specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.
Tiburcio AF, Altabella T, Bitrián M, Alcázar R. 2014. The role of polyamines during the lifespan of plants: from development to stress. Planta 240: 1–18.
Vera‐Sirera F, De Rybel B, Úrbez C, Kouklas E, Pesquera M, Álvarez‐Mahecha JC, Minguet EG, Tuominen H, Carbonell J, Borst JW et al. 2015. A bHLH‐based feedback loop restricts vascular cell proliferation in plants. Developmental Cell 35: 432–443.
معلومات مُعتمدة: JP23K05231 JSPS KAKENHI
فهرسة مساهمة: Keywords: ACL5; Selaginella moellendorffii; aminopropyltransferase; norspermine; polyamine; substrate specificity; thermospermine
المشرفين على المادة: 70862-11-2 (thermospermine)
2FZ7Y3VOQX (Spermine)
0 (Plant Proteins)
تواريخ الأحداث: Date Created: 20240408 Date Completed: 20240523 Latest Revision: 20240523
رمز التحديث: 20240523
DOI: 10.1111/nph.19733
PMID: 38587066
قاعدة البيانات: MEDLINE
الوصف
تدمد:1469-8137
DOI:10.1111/nph.19733