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Increase in ENHANCER OF SHOOT REGENERATION2 expression by treatment with strigolactone-related inhibitors and kinetin during adventitious shoot formation in ipecac

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Increase of ENHANCER OF SHOOT REGENERATION 2 expression was consistent to treatment with kinetin, TIS108, and KK094 in adventitious shoot formation of ipecac.

Abstract

Unlike many plant species, ipecac (Carapichea ipecacuanha (Brot.) L. Andersson) can form adventitious shoots in tissue culture without cytokinin (CK) treatment. Strigolactone (SL) biosynthesis and signaling inhibitors stimulate adventitious shoot formation in ipecac, suggesting their potential use as novel growth regulators in plant tissue culture, but the molecular mechanism of their action is unclear. In this study, we compared the effects of SL-related inhibitors (TIS108 and KK094) and CKs (2iP, tZ, and kinetin) on adventitious shoot formation in ipecac. Exogenously applied SL-related inhibitors and CKs stimulated adventitious shoot formation. Combinations of SL-related inhibitors and kinetin also promoted adventitious shoot formation, but without additive effects. We also analyzed the expression of CK biosynthesis genes in ipecac. TIS108 increased the expression of the ipecac homolog of ISOPENTENYL TRANSFERASE 3 (CiIPT3) but decreased that of LONELY GUY 7 homolog (CiLOG7), presumably resulting in no change in 2iP-type CK levels. KK094 and kinetin increased CiLOG7 expression, elevating 2iP-type CK levels. Among pluripotency- and meristem-related genes, TIS108, KK094, and kinetin consistently increased the expression of ENHANCER OF SHOOT REGENERATION 2 homolog (CiESR2), which has a key role in shoot regeneration, in the internodal segment region that formed adventitious shoots. We propose that CiESR2 might be a key stimulator of adventitious shoot formation in ipecac.

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All data generated or analysed during this study are included in this published article and its supplementary information files.

References

  • Abe S, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, Kim HI, Yoneyama K, Xie X, Ohnishi T, Seto Y, Yamaguchi S, Akiyama K, Yoneyama K, Nomura T (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci USA 111:18084–18089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y-S, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  CAS  PubMed  Google Scholar 

  • Aremu AO, Plačková L, Bairu MW, Novák O, Szüčová L, Doležal K, Finnie JF, Van Staden J (2014) Endogenous cytokinin profiles of tissue-cultured and acclimatized ‘Williams’ bananas subjected to different aromatic cytokinin treatments. Plant Sci 214:88–98

    Article  CAS  PubMed  Google Scholar 

  • Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Muller D, Domagalska MA, Leyser O (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137:2905–2913

    Article  CAS  PubMed  Google Scholar 

  • Daimon Y, Takabe K, Tasaka M (2003) The CUP-SHAPED COTYLEDON genes promote adventitious shoot formation on calli. Plant Cell Physiol 44:113–121

    Article  CAS  PubMed  Google Scholar 

  • Evans DA, Sharp WR, Flick CE (1981) Growth and behavior of cell cultures: Embryogenesis and organogenesis. In: Thorpe TA (ed) Plant tissue culture: methods and applications in agriculture. Academic Press, New York, pp 45–113

    Chapter  Google Scholar 

  • Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158

    Article  CAS  PubMed  Google Scholar 

  • Ideda K, Teshima D, Aoyama T, Satake M, Shimomura K (1988) Clonal propagation of Cephaelis ipecacuanha. Plant Cell Rep 7:288–291

    Article  CAS  PubMed  Google Scholar 

  • Ikeda Y, Banno H, Niu Q-W, Howell SH, Chua N-H (2006) The ENHANCER OF SHOOT REGENERATION 2 gene in Arabidopsis regulates CUP-SHAPED COTYLEDON 1 at the transcriptional level and controls cotyledon development. Plant Cell Physiol 47:1443–1456

    Article  CAS  PubMed  Google Scholar 

  • Ikeuchi M, Favero DS, Sakamoto Y, Iwase A, Coleman D, Rymen B, Sugimoto K (2019) Molecular mechanisms of plant regeneration. Annu Rev Plant Biol 70:377–406

    Article  CAS  PubMed  Google Scholar 

  • Ito S, Umehara M, Hanada A, Kitahata N, Hayase H, Yamaguchi S, Asami T (2011) Effects of triazole derivatives on strigolactone levels and growth retardation in rice. PLoS ONE 6:e21723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito S, Umehara M, Hanada A, Yamaguchi S, Asami T (2013) Effects of strigolactone-biosynthesis inhibitor TIS108 on Arabidopsis. Plant Signal Behav 8:e24193

    Article  PubMed  PubMed Central  Google Scholar 

  • Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685

    Article  CAS  PubMed  Google Scholar 

  • Kareem A, Durgaprasad K, Sugimoto K, Du Y, Pulianmackal AJ, Trivedi ZB, Abhayadev PV, Pinon V, Meyerowitz EM, Scheres B, Prasad K (2015) PLETHORA genes control regeneration by a two-step mechanism. Curr Biol 25:1017–1030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koike I, Taniguchi K, Shimomura K, Umehara M (2017) Dynamics of endogenous indole-3-acetic acid and cytokinins during adventitious shoot formation in ipecac. J Plant Growth Regul 36:805–813

    Article  CAS  Google Scholar 

  • Koike I, Watanabe S, Okazaki K, Hayashi KI, Kasahara H, Shimomura K, Umehara M (2020) Endogenous auxin determines the pattern of adventitious shoot formation on internodal segments of ipecac. Planta 251:73

    Article  CAS  PubMed  Google Scholar 

  • Koike I, Shimomura K, Umehara M (2018) Quantification of endogenous auxin and cytokinin during internode culture of ipecac. J Vis Exp e56902

  • Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H (2009) Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21:3152–3169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HW, Kim NY, Lee DJ, Kim J (2009) LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiol 151:1377–1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuo N, Makino M, Banno H (2011) Arabidopsis ENHANCER OF SHOOT REGENERATION (ESR)1 and ESR2 regulate in vitro shoot regeneration and their expressions are differentially regulated. Plant Sci 181:39–46

    Article  CAS  PubMed  Google Scholar 

  • Menges M, Samland AK, Sv P, Murray JAH (2006) The D-type cyclin CYCD3;1 Is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell 18:893–906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller CO, Skoog F, Von Saltza MH, Strong FM (1955) Kinetin, a cell division factor from deoxyribonucleic acid. J Am Chem Soc 77:1392–1392

    Article  CAS  Google Scholar 

  • Nakamura H, Hirabayashi K, Miyakawa T, Kikuzato K, Hu W, Xu Y, Jiang K, Takahashi I, Niiyama R, Dohmae N, Tanokura M, Asami T (2019) Triazole ureas covalently bind to strigolactone receptor and antagonize strigolactone responses. Mol Plant 12:44–58

    Article  CAS  PubMed  Google Scholar 

  • Okazaki K, Watanabe S, Koike I, Kawada K, Ito S, Nakamura H, Asami T, Shimomura K, Umehara M (2021) Strigolactone signaling inhibition increases adventitious shoot formation on internodal segments of ipecac. Planta 253:123

    Article  CAS  PubMed  Google Scholar 

  • Okazaki K, Koike I, Kera S, Yamaguchi K, Shigenobu S, Shimomura K, Umehara M (2022) Gene expression profiling before and after internode culture for adventitious shoot formation in ipecac. BMC Plant Biol 22:361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: Unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmülling T, Werner T, Riefler M, Krupková E, Bartrina y Manns I, (2003) Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J Plant Res 116:241–252

    Article  PubMed  Google Scholar 

  • Shuai B, Reynaga-Peña CG, Springer PS (2002) The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol 129:747–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skirycz A, Radziejwoski A, Busch W, Hannah MA, Czeszejko J, Kwaśniewski M, Zanor MI, Lohmann JU, De Veylder L, Witt I, Mueller-Roeber B (2008) The DOF transcription factor OBP1 is involved in cell cycle regulation in Arabidopsis thaliana. Plant J 56:779–792

    Article  CAS  PubMed  Google Scholar 

  • Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11:118–130

    CAS  PubMed  Google Scholar 

  • Takei K, Sakakibara H, Sugiyama T (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J Biol Chem 276:26405–26410

    Article  CAS  PubMed  Google Scholar 

  • Takei K, Yamaya T, Sakakibara H (2004) Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-Zeatin. J Biol Chem 279:41866–41872

    Article  CAS  PubMed  Google Scholar 

  • Yoshimatsu K, Shimomura K (1991) Efficient shoot formation on internodal segments and alkaloid formation in the regenerates of Cephaelis ipecacuanha A. Richard Plant Cell Rep 9:567–570

    CAS  PubMed  Google Scholar 

  • Zhai N, Xu L (2021) Pluripotency acquisition in the middle cell layer of callus is required for organ regeneration. Nature Plants 7:1453–1460

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Chen Y, Lin X, Hong X, Zhu Y, Li W, He W, An F, Guo H (2013) Adenine phosphoribosyl transferase 1 is a key enzyme catalyzing cytokinin conversion from nucleobases to nucleotides in Arabidopsis. Mol Plant 6:1661–1672

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

In 2001, regenerated ipecac plants were kindly provided by the Tsukuba Division, Research Center for Medicinal Plant Resources, National Institutes of Biomedical Innovation, Health and Nutrition, Japan. We thank Ms. Yuko Amagai, Toyo University, for technical support in plant tissue culture, and Prof. Hirobumi Yamamoto, Toyo University, for constructive comments on this study.

Funding

This study was in part supported by the Inoue Enryo Memorial Foundation for Promoting Science from Toyo University to KO, the Sasagawa Scientific Research Grant from The Japan Science Society to KO (2022–4085), JST SPRING to KO (JPMJSP2159), Grant-in-Aid for JSPS Fellows from Japan Society for the Promotion of Science to KO (23KJ1980), Program for Promotion of Practical Use of Intellectual Property from Toyo University to MU, and the 30th and 31st Botanical Research Grants from Ichimura Foundation for New Technology to MU.

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Authors and Affiliations

  1. Graduate School of Life Sciences, Toyo University, 1-1-1 Izumino, Itakura-Machi, Ora-Gun, Gunma, 374-0193, Japan

    Karin Okazaki, Koichiro Shimomura & Mikihisa Umehara

  2. Department of Bioscience, Tokyo University of Agriculture, 1-1-1 Sakuragaoka, Setagaya, Tokyo, 156-8502, Japan

    Shinsaku Ito

  3. Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo, 113-8657, Japan

    Hidemitsu Nakamura & Tadao Asami

Authors
  1. Karin Okazaki
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  2. Shinsaku Ito
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  3. Hidemitsu Nakamura
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  4. Tadao Asami
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  5. Koichiro Shimomura
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  6. Mikihisa Umehara
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Contributions

KO and MU conceived and designed the research. KS provided sterile ipecac plants. KO conducted the ipecac tissue culture experiments. SI and TA synthesized TIS108. HN and TA synthesized KK094. KO and MU analyzed the data. KO, KS, and MU wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Mikihisa Umehara.

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Communicated by Fumihiko Sato.

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Okazaki, K., Ito, S., Nakamura, H. et al. Increase in ENHANCER OF SHOOT REGENERATION2 expression by treatment with strigolactone-related inhibitors and kinetin during adventitious shoot formation in ipecac. Plant Cell Rep 42, 1927–1936 (2023). https://doi.org/10.1007/s00299-023-03073-y

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