Increase in ENHANCER OF SHOOT REGENERATION2 expression by treatment with strigolactone-related inhibitors and kinetin during adventitious shoot formation in ipecac.
Adventitious shoot
Carapichea ipecacuanha
KK094
Kinetin
TIS108
Journal
Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
01
09
2023
accepted:
18
09
2023
medline:
13
11
2023
pubmed:
7
10
2023
entrez:
6
10
2023
Statut:
ppublish
Résumé
Increase of ENHANCER OF SHOOT REGENERATION 2 expression was consistent to treatment with kinetin, TIS108, and KK094 in adventitious shoot formation of ipecac. 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.
Identifiants
pubmed: 37803214
doi: 10.1007/s00299-023-03073-y
pii: 10.1007/s00299-023-03073-y
doi:
Substances chimiques
Kinetin
P39Y9652YJ
Ipecac
8012-96-2
GR24 strigolactone
0
Cytokinins
0
Plant Growth Regulators
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1927-1936Subventions
Organisme : Toyo University
ID : Inoue Enryo Memorial Foundation for Promoting Science
Organisme : Toyo University
ID : Program for Promotion of Practical Use of Intellectual Property
Organisme : Japan Science Society
ID : 2022-4085
Organisme : Japan Science and Technology Agency
ID : JPMJSP2159
Organisme : Ichimura Foundation of New Technology
ID : the 30th
Organisme : Ichimura Foundation of New Technology
ID : 31st Botanical Research Grants
Organisme : Japan Society for the Promotion of Science
ID : 23KJ1980
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
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
doi: 10.1073/pnas.1410801111
pubmed: 25425668
pmcid: 4273391
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
doi: 10.1105/tpc.9.6.841
pubmed: 9212461
pmcid: 156962
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
doi: 10.1016/j.cell.2004.09.018
pubmed: 15454085
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
doi: 10.1016/j.plantsci.2013.09.012
pubmed: 24268166
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
doi: 10.1242/dev.051987
pubmed: 20667910
Daimon Y, Takabe K, Tasaka M (2003) The CUP-SHAPED COTYLEDON genes promote adventitious shoot formation on calli. Plant Cell Physiol 44:113–121
doi: 10.1093/pcp/pcg038
pubmed: 12610213
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
doi: 10.1016/B978-0-12-690680-6.50008-5
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158
doi: 10.1016/0014-4827(68)90403-5
pubmed: 5650857
Ideda K, Teshima D, Aoyama T, Satake M, Shimomura K (1988) Clonal propagation of Cephaelis ipecacuanha. Plant Cell Rep 7:288–291
doi: 10.1007/BF00272545
pubmed: 24241769
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
doi: 10.1093/pcp/pcl023
pubmed: 17056621
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
doi: 10.1146/annurev-arplant-050718-100434
pubmed: 30786238
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
doi: 10.1371/journal.pone.0021723
pubmed: 21760901
pmcid: 3132747
Ito S, Umehara M, Hanada A, Yamaguchi S, Asami T (2013) Effects of strigolactone-biosynthesis inhibitor TIS108 on Arabidopsis. Plant Signal Behav 8:e24193
doi: 10.4161/psb.24193
pubmed: 23511201
pmcid: 3907539
Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685
doi: 10.1093/pcp/pce112
pubmed: 11479373
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
doi: 10.1016/j.cub.2015.02.022
pubmed: 25819565
pmcid: 4829346
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
doi: 10.1007/s00344-017-9684-8
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
doi: 10.1007/s00425-020-03367-5
pubmed: 32140780
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
doi: 10.1105/tpc.109.068676
pubmed: 19837870
pmcid: 2782294
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
doi: 10.1104/pp.109.143685
pubmed: 19717544
pmcid: 2773067
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
doi: 10.1016/j.plantsci.2011.03.007
pubmed: 21600396
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
doi: 10.1105/tpc.105.039636
pubmed: 16517759
pmcid: 1425856
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
doi: 10.1021/ja01610a105
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
doi: 10.1016/j.molp.2018.10.006
pubmed: 30391752
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
doi: 10.1007/s00425-021-03640-1
pubmed: 34014387
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
doi: 10.1186/s12870-022-03756-w
pubmed: 35869421
pmcid: 9308184
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
doi: 10.1105/tpc.104.028316
pubmed: 15659631
pmcid: 548818
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
doi: 10.1007/s10265-003-0096-4
pubmed: 12721786
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
doi: 10.1104/pp.010926
pubmed: 12068116
pmcid: 161698
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
doi: 10.1111/j.1365-313X.2008.03641.x
pubmed: 18665917
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
pubmed: 13486467
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
doi: 10.1074/jbc.M102130200
pubmed: 11313355
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
doi: 10.1074/jbc.M406337200
pubmed: 15280363
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
pubmed: 24220713
Zhai N, Xu L (2021) Pluripotency acquisition in the middle cell layer of callus is required for organ regeneration. Nature Plants 7:1453–1460
doi: 10.1038/s41477-021-01015-8
pubmed: 34782770
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
doi: 10.1093/mp/sst071
pubmed: 23658065