Abstract
Trichoderma is an important genus of symbiotic fungi, commonly used around the world as biocontrol agents and as biofertilizer. Although their beneficial effects are well known and are successfully exploited in sustainable agriculture practices, the biochemical mechanisms of plant growth-promoting actions of Trichoderma and their anti-pathogen characteristics are not well understood. This study biochemically surveyed 22 strains of Trichoderma and shows that Trichoderma produces cytokinins (CKs), which has not been reported to date. The phytohormone profiles ranged from 5.34 to 379.99 pmol CKs released to 10 mL of the growth medium and comprised riboside and nucleotide derivatives of cis-zeatin (cZ) and isopentenyladenine (iP), suggesting that fungal CKs originate from a tRNA degradation pathway. We reveal a connection between the levels of free base cZ produced by Trichoderma and the inhibition rate against the pathogen Fusarium graminearum among the tested strains. Furthermore, we analyzed CK profiles of Arabidopsis plants cultured in vitro in the presence of Trichoderma strains. The inoculated plants showed increased levels of cZ-type (cZR, cZROG) and iP-type (iP, iPR) CKs—the forms which dominated CK profiles of all the fungal in vitro cultures tested in this study. The increase in the levels of cZ derivatives was accompanied by a significant reduction in plant trans-zeatin (tZ)-type CKs (tZR, tZNT, tZOG, tZ7G, tZ9G) in Arabidopsis when co-cultured with the fungus. Our work suggests that CKs produced by plant symbiotic Trichoderma strains can be used for plant growth stimulation, may impact the colonization strategy of symbiotic fungi, and include alterations to the host plant phytohormones for enhanced plant resistance against pathogens.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abo Nouh FA (2019) Endophytic fungi for sustainable agriculture. Microbiol Biosyst 4:31–44. https://doi.org/10.21608/MB.2019.38886
Akagi A, Fukushima S, Okada K, Jiang CJ, Yoshida R, Nakayama A, Shimono M, Sugano M, Yamane H, Takatsuji H (2014) WRKY45-dependent priming of diterpenoid phytoalexin biosynthesis in rice and the role of cytokinin in triggering the reaction. Plant Mol Biol 86:171–183. https://doi.org/10.1007/s11103-014-0221-x
Akhtar SS, Mekureyaw MF, Pandey C, Roitsch T (2019) Role of cytokinins for interactions of plants with microbial pathogens and pest insects. Front Plant Sci 10:1777. https://doi.org/10.3389/fpls.2019.01777
Akhter W, Bhuiyan MKA, Sultana F, Hossain MM (2015) Integrated effect of microbial antagonist, organic amendment and fungicide in controlling seedling mortality (Rhizoctonia solani) and improving yield in pea (Pisum sativum L.). CR Biol 338:21–28. https://doi.org/10.1016/j.crvi.2014.10.003
Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2:1–12. https://doi.org/10.2478/v10102-009-0001-7
Allen MF, Moore TS Jr, Christensen M (1980) Phytohormone changes in Bouteloua gracilis infected by vesicular–arbuscular mycorrhizae: I. Cytokinin increases in the host plant. Can J Bot 58:371–374. https://doi.org/10.1139/b80-038
Aoki MM, Seegobin M, Kisiala A, Noble A, Brunetti C, Emery RJN (2019) Phytohormone metabolism in human cells: cytokinins are taken up and interconverted in HeLa cell culture. FASEB BioAdv 1:320–331. https://doi.org/10.1096/fba.2018-00032
Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR (2005) Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 272:201–209. https://doi.org/10.1007/s11104-004-5047-x
Arkhipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315. https://doi.org/10.1007/s11104-007-9233-5
Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745. https://doi.org/10.1126/science.1113373
Atkins CA, Pigeaire A (1993) Application of cytokinins to flowers to increase pod set in Lupinus angustifolius L. Aust J Agric Res 44:1799–1819. https://doi.org/10.1071/AR9931799
Babosha AV (2009) Regulation of resistance and susceptibility in wheat–powdery mildew pathosystem with exogenous cytokinins. J Plant Physiol 166:1892–1903. https://doi.org/10.1016/j.jplph.2009.05.014
Bompadre MJ, Bidondo LF, Silvani VA, Colombo RP, Pérgola M, Pardo AG, Godeas AM (2015) Combined effects of arbuscular mycorrhizal fungi and exogenous cytokinins on pomegranate (Punica granatum) under two contrasting water availability conditions. Symbiosis 65:55–63. https://doi.org/10.1007/s13199-015-0318-2
Bozcuk S (1981) Effects of kinetin and salinity on germination of tomato, barley and cotton seeds. Ann Bot 48:81–84. https://doi.org/10.1093/oxfordjournals.aob.a086100
Chanclud E, Kisiala A, Emery NR, Chalvon V, Ducasse A, Romiti-Michel C, Gravot A, Kroj T, Morel JB (2016) Cytokinin production by the rice blast fungus is a pivotal requirement for full virulence. PLoS Path https://doi.org/10.1371/journal.ppat.1005457
Checker VG, Kushwaha HR, Kumari P, Yadav S (2018) Role of phytohormones in plant defense: signaling and cross talk. In: Singh A, Singh I (eds) Molecular aspects of plant-pathogen interaction. Springer, Singapore
Choi J, Huh SU, Kojima M, Sakakibara H, Paek KH, Hwang I (2010) The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev Cell 19:284–295. https://doi.org/10.1016/j.devcel.2010.07.011
Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C, López-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592. https://doi.org/10.1104/pp.108.130369
Contreras-Cornejo HA, Macías-Rodríguez L, Vergara AG, López-Bucio J (2015) Trichoderma modulates stomatal aperture and leaf transpiration through an abscisic acid-dependent mechanism in Arabidopsis. J Plant Growth Regul 34:425–432. https://doi.org/10.1007/s00344-014-9471-8
Contreras-Cornejo HA, Macías-Rodríguez L, del-Val E, Larsen J (2016) Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiol Ecol 92:36. https://doi.org/10.1093/femsec/fiw036
Cosme M, Ramireddy E, Franken P, Schmülling T, Wurst S (2016) Shoot- and root-borne cytokinin influences arbuscular mycorrhizal symbiosis. Mycorrhiza 26:709–720. https://doi.org/10.1007/s00572-016-0706-3
Dervinis C, Frost CJ, Lawrence SD, Novak NG, Davis JM (2010) Cytokinin primes plant responses to wounding and reduces insect performance. J Plant Growth Regul 29:289–296. https://doi.org/10.1007/s00344-009-9135-2
Eddleman H (1998) Making bacteria media from potato. Indiana Biolab. https://www.disknet.com. Retrieved 4 Apr 2011.
Eisermann I, Motyka V, Kümmel S, Dobrev PI, Hübner K, Deising HB, Wirsel SG (2020) CgIPT1 is required for synthesis of cis-zeatin cytokinins and contributes to stress tolerance and virulence in Colletotrichum graminicola. Fungal Gen Biol 143:103436. https://doi.org/10.1016/j.fgb.2020.103436
El Mansy SM, Fatma Ahmed Abo Nouh FA, Mousa MK, Abdel-Azeem AM (2020) Endophytic fungi: diversity, abundance, and plant growth-promoting attributes. In: Mishra S, Kour D, Yadav N, Kumar A, Yadav A (eds) Agriculturally important fungi for sustainable agriculture. Fungal biology. Springer, Cham
Egamberdieva D, Wirth SJ, Alqarawi AA, Abd Allah EF, Hashem A (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8:2104. https://doi.org/10.3389/fmicb.2017.02104
FAO (2017) The future of food and agriculture—trends and challenges. Rome. http://www.fao.org/3/a-i6583e.pdf. Accessed 26 June 2020
Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452. https://doi.org/10.1093/jxb/err004
Gamar MIA, Kisiala A, Emery RJN, Yeung EC, Stone SL, Qaderi MM (2019) Elevated carbon dioxide decreases the adverse effects of higher temperature and drought stress by mitigating oxidative stress and improving water status in Arabidopsis thaliana. Planta 250:1191–1214. https://doi.org/10.1007/s00425-019-03213-3
Gibb M, Kisiala AB, Morrison EN, Emery RJN (2020) The origins and roles of methylthiolated cytokinins: evidence from among life kingdoms. Front Cell Dev Biol 8:605672. https://doi.org/10.3389/fcell.2020.605672
Goh DM, Cosme M, Kisiala AB, Mulholland S, Said ZM, Spichal L, Emery RJN, Declerck S, Guinel FC (2019) A stimulatory role for cytokinin in the arbuscular mycorrhizal symbiosis of pea. Front Plant Sci 10:262. https://doi.org/10.3389/fpls.2019.00262
Goyal A, Kalia A (2020) Fungal phytohormones: plant growth-regulating substances and their applications in crop productivity. In: Mishra S, Kour D, Yadav N, Kumar A, Yadav A (eds) Agriculturally important fungi for sustainable agriculture. Fungal biology. Springer, Cham
Großkinsky D, Edelsbrunner K, Pfeifhofer H, Van der Graaff E, Roitsch T (2013) Cis-and trans-zeatin differentially modulate plant immunity. Plant Signal Behav 8:e24798. https://doi.org/10.4161/psb.24798
Großkinsky DK, Tafner R, Moreno MV, Stenglein SA, De Salamone IEG, Nelson LM, Novák O, Strnad M, van der Graaff E, Roitsch T (2016) Cytokinin production by Pseudomonas fluorescens G20–18 determines biocontrol activity against Pseudomonas syringae in Arabidopsis. Sci Rep 6:23310. https://doi.org/10.1038/srep23310
Gupta R, Pizarro L, Leibman-Markus M, Marash I, Bar M (2020) Cytokinin response induces immunity and fungal pathogen resistance, and modulates trafficking of the PRR LeEIX2 in tomato. Mol Plant Pathol 21:1287–1306. https://doi.org/10.1101/2020.03.23.003822
Guzmán-Guzmán P, Porras-Troncoso MD, Olmedo-Monfil V, Herrera-Estrella A (2019) Trichoderma species: versatile plant symbionts. Phytopathology 109:6–16. https://doi.org/10.1094/PHYTO-07-18-0218-RVW
Haque MM, Ilias GNM, Molla AH (2012) Impact of Trichoderma-enriched biofertilizer on the growth and yield of mustard (Brassica rapa L.) and tomato (Solanum lycopersicon Mill.). Agriculturists 10:109–119. https://doi.org/10.3329/agric.v10i2.13148
Hinsch J, Vrabka J, Oeser B, Novák O, Galuszka P, Tudzynski P (2015) De novo biosynthesis of cytokinins in the biotrophic fungus Claviceps purpurea. Env Microbiol 17:2935–2951. https://doi.org/10.1111/1462-2920.12838
Jameson PE, Song J (2016) Cytokinin: a key driver of seed yield. J Exp Bot 67:593–606. https://doi.org/10.1093/jxb/erv461
Jiang CJ, Shimono M, Sugano S, Kojima M, Liu X, Inoue H, Sakakibara H, Takatsuji H (2013) Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice. MPMI 26:287–296. https://doi.org/10.1094/MPMI-06-12-0152-R
Jorge GL, Kisiala A, Morrison E, Aoki M, Nogueira APO, Emery RJN (2019) Endosymbiotic Methylobacterium oryzae mitigates the impact of limited water availability in lentil (Lens culinaris Medik.) by increasing plant cytokinin levels. Env Exp Bot 162:525–540. https://doi.org/10.1016/j.envexpbot.2019.03.028
Kambhampati S, Kurepin LV, Kisiala AB, Bruce KE, Cober ER, Morrison MJ, Emery RJN (2017) Yield associated traits correlate with cytokinin profiles in developing pods and seeds of field-grown soybean cultivars. Field Crops Res 214:175–184. https://doi.org/10.1016/j.fcr.2017.09.009
Karnwal A, Kaushik P (2011) Cytokinin production by fluorescent Pseudomonas in the presence of rice root exudates. Arch Phytopathology Plant Protect 44:1728–1735. https://doi.org/10.1080/03235408.2010.526768
Kieber JJ, Schaller GE (2014) Cytokinins. The Arabidopsis Book/ASPB. https://doi.org/10.1199/tab.0168
Kisiala A, Laffont C, Emery RJN, Frugier F (2013) Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonnodulating strains. MPMI 26:1225–1231. https://doi.org/10.1094/MPMI-02-13-0054-R
Kisiala A, Kambhampati S, Stock NL, Aoki M, Emery RJN (2019) Quantification of cytokinins using high-resolution accurate-mass orbitrap mass spectrometry and parallel reaction monitoring (PRM). Anal Chem 91:15049–15056. https://doi.org/10.1021/acs.analchem.9b03728
Kudoyarova GR, Melentiev AI, Martynenko EV, Timergalina LN, Arkhipova TN, Shendel GV, Kuz’mina LY, Dodd IC, Veselov SY (2014) Cytokinin producing bacteria stimulate amino acid deposition by wheat roots. Plant Physiol Biochem 83:285–291. https://doi.org/10.1016/j.plaphy.2014.08.015
Kudoyarova G, Arkhipova TN, Korshunova T, Bakaeva M, Loginov O, Dodd IC (2019) Phytohormone mediation of interactions between plants and non-symbiotic growth promoting bacteria under edaphic stresses. Front Plant Sci 10:1368. https://doi.org/10.3389/fpls.2019.01368
Liu F, Xing S, Ma H, Du Z, Ma B (2013) Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotech 97:9155–9164. https://doi.org/10.1007/s00253-013-5193-2
Macías-Rodríguez L, Guzmán-Gómez A, García-Juárez P, Contreras-Cornejo HA (2018) Trichoderma atroviride promotes tomato development and alters the root exudation of carbohydrates, which stimulates fungal growth and the biocontrol of the phytopathogen Phytophthora cinnamomi in a tripartite interaction system. FEMS Microbiol Ecol 94:fiy137
Macías-Rodríguez L, Contreras-Cornejo HA, Adame-Garnica SG, Del-Val E, Larsen J (2020) The interactions of Trichoderma at multiple trophic levels: inter-kingdom communication. Microbiol Res. https://doi.org/10.1016/j.micres.2020.126552
Macková H, Hronková M, Dobrá J, Turečková V, Novák O, Lubovská Z, Motyka V, Haisel D, Hájek T, Prášil IT, Gaudinová A, Štorchová H, Ge E, Werner T, Schmülling T, Gaudinová A (2013) Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J Exp Bot 64:2805–2815. https://doi.org/10.1093/jxb/ert131
Martínez-Medina A, Alguacil MDM, Pascual JA, Van Wees SC (2014) Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. J Chem Ecol 40:804–815. https://doi.org/10.1007/s10886-014-0478-1
Morrison EN, Emery RJN, Saville BJ (2017) Fungal derived cytokinins are necessary for normal Ustilago maydis infection of maize. Plant Pathol 66:726–742. https://doi.org/10.1111/ppa.12629
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Olmedo V, Casas-Flores S (2014) Chapter 32 - Molecular mechanisms of biocontrol in Trichoderma spp and their applications in agriculture. In: Gupta VK, Schmoll M et al (eds) Biotechnology and biology of trichoderma. Elsevier, Amsterdam
Pan H, Chen M, Feng H, Wei M, Song F, Lou Y, Cuia X, Wang H, Zhuge Y (2020) Organic and inorganic fertilizers respectively drive bacterial and fungal community compositions in a fluvo-aquic soil in northern China. Soil Tillage Res 198:104540. https://doi.org/10.1016/j.still.2019.104540
Patel T, Saraf M (2017) Biosynthesis of phytohormones from novel rhizobacterial isolates and their in vitro plant growth-promoting efficacy. J Plant Interact 12:480–487. https://doi.org/10.1080/17429145.2017.1392625
Persson BC, Björk GR (1993) Isolation of the gene (miaE) encoding the hydroxylase involved in the synthesis of 2-methylthio-cis-ribozeatin in tRNA of Salmonella typhimurium and characterization of mutants. J Bacteriol 175:7776–7785. https://doi.org/10.1128/jb.175.24.7776-7785.1993
Pertry I, Vaclavikova K, Depudt S, Galuszka P, Spichal L, Temmerman W, Stes E, Schmülling T, Kakimoto T, Van Montagu MCE, Strnad M, Holsters M, Tarkowski M, Vereecke D (2009) Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc Natl Acad Sci USA 106:929–934. https://doi.org/10.1073/pnas.0811683106
Pons S, Fournier S, Chervin C, Bécard G, Rochange S, Frei Dit Frey N, Puech Pagès V (2020) Phytohormone production by the arbuscular mycorrhizal fungus Rhizophagus irregularis. PLoS ONE 15:e0240886. https://doi.org/10.1371/journal.pone.0240886
Powell AF, Paleczny AR, Olechowski H, Emery RJN (2013) Changes in cytokinin form and concentration in developing kernels correspond with variation in yield among field-grown barley cultivars. Plant Physiol Biochem 64:33–40. https://doi.org/10.1016/j.plaphy.2012.12.010
Rubio MB, Quijada NM, Pérez E, Domínguez S, Monte E, Hermosa R (2014) Identifying beneficial qualities of Trichoderma parareesei for plants. Appl Environ Microbiol 80:1864–1873. https://doi.org/10.1128/AEM.03375-13
Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449. https://doi.org/10.1146/annurev.arplant.57.032905.105231
Salas-Marina MA, Silva-Flores MA, Cervantes-Badillo MG, Rosales-Saavedra MT, Islas-Osuna MA, Casas-Flores S (2011) The plant growth-promoting fungus Aspergillus ustus promotes growth and induces resistance against different lifestyle pathogens in Arabidopsis thaliana. J Microbiol Biotechn 21:686–696. https://doi.org/10.4014/jmb.1101.01012
Sáenz-Mata J, Jiménez-Bremont JF (2012) HR4 gene is induced in the Arabidopsis-Trichoderma atroviride beneficial interaction. Int J Mol Sci 13:9110–9128. https://doi.org/10.3390/ijms13079110
Schäfer M, Brütting C, Meza-Canales ID, Großkinsky DK, Vankova R, Baldwin IT, Meldau S (2015) The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions. J Exp Bot 66:4873–4884. https://doi.org/10.1093/jxb/erv214
Shigenaga AM, Argueso CT (2016) No hormone to rule them all: Interactions of plant hormones during the responses of plants to pathogens. Semin Cell Dev Biol 56:174–189. https://doi.org/10.1016/j.semcdb.2016.06.005
Sood M, Kapoor D, Kumar V, Sheteiwy MS, Ramakrishnan M, Araniti LM, F, Sharma A (2020) Trichoderma: the “secrets” of a multitalented biocontrol agent. Plants 9:762. https://doi.org/10.3390/plants9060762
Srivastava SN, Singh V, Awasthi SK (2006) Trichoderma induced improvement in growth, yield and quality of sugarcane. Sugar Tech 8:166–169. https://doi.org/10.1007/BF02943654
Singh S, Prasad SM (2014) Growth, photosynthesis and oxidative responses of Solanum melongena L. seedlings to cadmium stress: mechanism of toxicity amelioration by kinetin. Sci Hort 176:1–10. https://doi.org/10.1016/j.scienta.2014.06.022
Stocco MC, Mónaco CI, Abramoff C, Lampugnani G, Salerno G, Kripelz N, Cordo CA, Consolo VF (2016) Selection and characterization of Argentine isolates of Trichoderma harzianum for effective biocontrol of Septoria leaf blotch of wheat. World J Microb Biot 32:49. https://doi.org/10.1007/s11274-015-1989-9
Trdá L, Barešová M, Šašek V, Nováková M, Zahajská L, Dobrev PI, Motyka V, Burketová L (2017) Cytokinin metabolism of pathogenic fungus Leptosphaeria maculans involves isopentenyltransferase, adenosine kinase and cytokinin oxidase/dehydrogenase. Front Microb 8:1374. https://doi.org/10.3389/fmicb.2017.01374
Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. MPMI 21:1371–1383. https://doi.org/10.1094/MPMI-21-10-1371
Vargas WA, Mandawe JC, Kenerley CM (2009) Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol 151:792–808. https://doi.org/10.1104/pp.109.141291
Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86. https://doi.org/10.1186/s12870-016-0771-y
Xue AG, Guo W, Chen Y, Siddiqui I, Marchand G, Liu J, Ren C (2017) Effect of seed treatment with novel strains of Trichoderma spp. on establishment and yield of spring wheat. Crop Prot 96:97–102. https://doi.org/10.1016/j.cropro.2017.02.003
Zalewski W, Galuszka P, Gasparis S, Orczyk W, Nadolska-Orczyk A (2010) Silencing of the HvCKX1 gene decreases the cytokinin oxidase/dehydrogenase level in barley and leads to higher plant productivity. J Exp Bot 61:1839–1851. https://doi.org/10.1093/jxb/erq052
Zhang P, Wang WQ, Zhang GL, Kaminek M, Dobrev P, Xu J, Gruissem W (2010) Senescence-inducible expression of isopentenyl transferase extends leaf life, increases drought stress resistance and alters cytokinin metabolism in cassava. J Integr Plant Biol 52:653–669. https://doi.org/10.1111/j.1744-7909.2010.00956.x
Zwack PJ, Rashotte AM (2015) Interactions between cytokinin signalling and abiotic stress responses. J Exp Bot 66:4863–4871. https://doi.org/10.1093/jxb/erv172
Acknowledgements
The authors thank Dr. Allen Xue from Ottawa Research and Development Centre, Agriculture and Agri-Food Canada for providing Trichoderma strains for the analysis. They also would like to thank Nourhène Grich for her assistance in growing Trichoderma strains and preparing fungal inoculum and Aaron Dain for his help in preparation of Arabidopsis in vitro cultures.
Funding
This work was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC Discovery Grant No: RGPIN-2018-05436 to RJNE) and a MITACS Globalink Research Internship to KMB.
Author information
Authors and Affiliations
Contributions
KMB, AK and RJNE contributed to the study conception and design. Material preparation, data collection and analysis were performed by KMB and AK. The first draft of the manuscript was written by KMB and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Handling Editor: Thomas Roitsch.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bean, K.M., Kisiala, A.B., Morrison, E.N. et al. Trichoderma Synthesizes Cytokinins and Alters Cytokinin Dynamics of Inoculated Arabidopsis Seedlings. J Plant Growth Regul 41, 2678–2694 (2022). https://doi.org/10.1007/s00344-021-10466-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-021-10466-4