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Micrococcus luteus LS570 promotes root branching in Arabidopsis via decreasing apical dominance of the primary root and an enhanced auxin response

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Abstract

The interaction of plant roots with bacteria is influenced by chemical signaling, where auxins play a critical role. Auxins exert positive or negative influences on the plant traits responsible of root architecture configuration such as root elongation and branching and root hair formation, but how bacteria that modify the plant auxin response promote or repress growth, as well as root structure, remains unknown. Here, we isolated and identified via molecular and electronic microscopy analysis a Micrococcus luteus LS570 strain as a plant growth promoter that halts primary root elongation in Arabidopsis seedlings and strongly triggers root branching and absorptive potential. The root biomass was exacerbated following root contact with bacterial streaks, and this correlated with inducible expression of auxin-related gene markers DR5:GUS and DR5:GFP. Cellular and structural analyses of root growth zones indicated that the bacterium inhibits both cell division and elongation within primary root tips, disrupting apical dominance, and as a consequence differentiation programs at the pericycle and epidermis, respectively, triggers the formation of longer and denser lateral roots and root hairs. Using Arabidopsis mutants defective on auxin signaling elements, our study uncovers a critical role of the auxin response factors ARF7 and ARF19, and canonical auxin receptors in mediating both the primary root and lateral root response to M. luteus LS570. Our report provides very basic information into how actinobacteria interact with plants and direct evidence that the bacterial genus Micrococcus influences the cellular and physiological plant programs ultimately responsible of biomass partitioning.

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References

  • Ahmad E, Sharma SK, Sharma PK (2020) Deciphering operation of tryptophan-independent pathway in high indole-3-acetic acid (IAA) producing Micrococcus aloeverae DCB-20. FEMS Microbiol Lett 367:fnaa190

    Article  CAS  PubMed  Google Scholar 

  • Artner C, Benkova E (2019) Ethylene and cytokinin: partners in root growth regulation. Mol Plant 12:1312–1314

    Article  CAS  PubMed  Google Scholar 

  • Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 9:1473

    Article  PubMed  PubMed Central  Google Scholar 

  • Busby PE, Soman C, Wagner MR, Friesen ML, Kremer J, Bennett A, Morsy M, Eisen JA, Leach JE, Dangl JL (2017) Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol 15(3):e2001793. Cell, 136: 1005-1016

  • Cox CE, Brandl MT, de Moraes MH, Gunasekera S, Teplitski M (2018) Production of the plant hormone auxin by Salmonella and its role in the interactions with plants and animals. Front Microbiol 8:2668

    Article  PubMed  PubMed Central  Google Scholar 

  • Dastager SG, Deepa CK, Pandey A (2010) Isolation and characterization of novel plant growth promoting Micrococcus sp NII-0909 and its interaction with cowpea. Plant Physiol Biochem 48:987–992

    Article  CAS  PubMed  Google Scholar 

  • Finkel OM, Salas-González I, Castrillo G, Conway JM, Law TF, Pereira Lima PJ, Wilson ED, Fitzpatrick CR, Jones CD, Dangl JL (2020) A single bacterial genus maintains root growth in a complex microbiome. Nature 587:103–108

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick CR, Salas-González I, Conway JM, Finkel OM, Gilbert S, Russ D, Teixeira PJPL, Dangl JL (2020) The plant microbiome: from ecology to reductionism and beyond. Annu Rev Microbiol 74:81–100

    Article  CAS  PubMed  Google Scholar 

  • Fu J, Wang S (2011) (2011) Insights into auxin signaling in plant-pathogen interactions. Front Plant Sci 2:74

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by again-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168

    Article  CAS  PubMed  Google Scholar 

  • Funes PMI, Salomon MV, Berli F, Gil R, Bottini R, Piccoli P (2018) Plant growth promoting rhizobacteria alleviate stress by AsIII in grapevine. Agric Ecosyst Environ 267:100–108

    Article  CAS  Google Scholar 

  • Ganin H, Kemper N, Meir S, Rogachev I, Ely S, Massalha H, Mandaby A, Shanzer A, Keren-Paz A, Meijler MM, Malitsky S, Aharoni A, Kolodkin-Gal I (2019) Indole derivatives maintain the status quo between beneficial biofilms and their plant hosts. Mol Plant-Microbe Interact 32:1013–1025

    Article  CAS  PubMed  Google Scholar 

  • Gilbert S, Xu J, Acosta K, Poulev A, Lebeis S, Lam E (2018) Bacterial production of indole related compounds reveals their role in association between duckweeds and endophytes. Front Chem 6:265

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • González-López O, Palacios-Nava B, Peña-Uribe CA, Campos-García J, López-Bucio J, García-Pineda E, Reyes de la Cruz H (2021) Growth promotion in Arabidopsis thaliana by bacterial cyclodipeptides involves the TOR/S6K pathway activation. J Plant Physiol 257:153343

    Article  PubMed  CAS  Google Scholar 

  • Gupta S, Pandey S (2019) ACC deaminase producing bacteria with multifarious plant growth promoting traits alleviates salinity stress in french bean (Phaseolus vulgaris) plants. Front Microbiol 10:1506

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang KL, Ma GJ, Zhang ML, Xiong H, Wu H, Zhao CZ, Liu CS, Jia HX, Chen L, Kjorven JO, Li XB, Ren F (2018) The ARF7 and ARF19 transcription factors positively regulate PHOSPHATE STARVATION RESPONSE1 in Arabidopsis Roots. Plant Physiol 178:413–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiménez-Vázquez KR, García-Cárdenas E, Barrera-Ortiz S, Ortiz-Castro R, Ruiz-Herrera LF, Ramos-Acosta BP, Coria-Arellano JL, Sáenz-Mata J, López-Bucio J (2020) The plant beneficial rhizobacterium Achromobacter sp. 5B1 influences root development through auxin signaling and redistribution. Plant J 103:1639–1654

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kunkel BN, Harper CP (2018) The roles of auxin during interactions between bacterial plant pathogens and their hosts. J Exp Bot 69(2):245–254

    Article  CAS  PubMed  Google Scholar 

  • Lee HW, Cho C, Pandey SK, Park Y, Kim MY, Kim J (2019) LBD16 and LBD18 acting downstream of ARF7 and ARF19 are involved in adventitious root formation in Arabidopsis. BMC Plant Biol 19:46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Méndez-Gómez M, Castro-Mercado E, Peña-Uribe CA, Reyes-de la Cruz H, López-Bucio J, García-Pineda E (2020) Azospirillum brasilense Sp245 lipopolysaccharides induce target of rapamycin signaling and growth in Arabidopsis thaliana. J Plant Physiol 253:153270

    Article  PubMed  CAS  Google Scholar 

  • Méndez-Gómez M, Barrera-Ortiz S, Castro-Mercado E, López-Bucio J, García-Pineda E (2021a) The nature of the interaction Azospirillum-Arabidopsis determines the molecular and morphological changes in root and plant growth promotion. Protoplasma 258:179–189

    Article  PubMed  CAS  Google Scholar 

  • Méndez-Gómez C-M, López-Bucio J, García-Pineda E (2021b) Azospirillum brasilense Sp245 triggers cytokinin signaling in root tips and improves biomass accumulation in Arabidopsis through canonical cytokinin receptors. Physiol Mol Biol Plants. https://doi.org/10.1007/s12298-021-01036-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Nascimento FX, Rossi MJ, Glick BR (2018) Ethylene and 1-aminocyclopropane-1 carboxylate (ACC) in plant–bacterial interactions. Front Plant Sci 9:114

    Article  PubMed  PubMed Central  Google Scholar 

  • Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortiz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujillo M, del Río R, Campos-García J, López-Bucio J (2011) Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Natl Acad Sci USA 108:7253–7258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortiz-Castro R, Pelagio-Flores R, Méndez Bravo A, Ruíz Herrera LF, Campos-García J, López-Bucio J (2014) Pyocyanin, a virulence factor produced by Pseudomonas aeruginosa, alters root development through reactive oxygen species and ethylene signaling in Arabidopsis. Mol Plant Microbe Interact 27:364–378

    Article  CAS  PubMed  Google Scholar 

  • Ortiz-Castro R, López-Bucio J (2019) Review: Phytostimulation and root architectural responses to quorum-sensing signals and related molecules from rhizobacteria. Plant Sci 284:135–142

    Article  CAS  PubMed  Google Scholar 

  • Ortiz-Castro R, Campos-García J, López-Bucio J (2020) Pseudomonas putida and Pseudomonas fluorescens influence Arabidopsis root system architecture through an auxin response mediated by bioactive cyclodipeptides. J Plant Growth Regul 39:254–265

    Article  CAS  Google Scholar 

  • Ottenschläger I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci USA 100:2987–2991

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pandey BK, Bennett MJ (2019) A new angle on how roots acclimate to sporadic rainfall. Cell 178:269–271

    Article  CAS  PubMed  Google Scholar 

  • Paque S, Weijers D (2016) Auxin: the plant molecule that influences almost anything. BMC Biol 14:67

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parry G, Calderón-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, Lechner E, Gray WM, Bennett M, Estelle M (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci USA 106:22540–22545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Flores P, Valencia-Cantero E, Altamirano-Hernández J, Pelagio-Flores R, López-Bucio J, García-Juárez P, Macías-Rodríguez L (2017) Bacillus methylotrophicus M4–96 isolated from maize (Zea mays) rhizoplane increases growth and auxin content in Arabidopsis thaliana via emission of volatiles. Protoplasma 254:2201–2213

    Article  PubMed  CAS  Google Scholar 

  • Prigge MJ, Platre M, Kadakia N, Zhang Y, Greenham K, Szutu W, Pandey BK, Bhosale RA, Bennett MJ, Busch W, Estelle M (2020) Genetic analysis of the Arabidopsis TIR1/AFB auxin receptors reveals both overlapping and specialized functions. Elife 9:e54740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin H, He HR (2019) The coordination of ethylene and other hormones in primary root development. Front Plant Sci 10:874

    Article  PubMed  PubMed Central  Google Scholar 

  • Raza FA, Faisal M (2013) Growth promotion of maize by desiccation tolerant Micrococcus luteus-chp37 isolated from Cholistan desert, Pakistan. Aust J Crop Sci 7:1693–1698

    Google Scholar 

  • Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M (1998) The TIR protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. Genes Dev 12:198–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salas-González I, Reyt G, Flis P, Custódio V, Gopaulchan D, Bakhoum N, Suresh K, Franke R, RB, Dangl JL, Salt DE, Castrillo G, (2021) Coordination between the microbiota and the root endodermis supports plant mineral nutrient homeostasis. Science 371:eabd0695

    Article  PubMed  CAS  Google Scholar 

  • Shishkova S, Rost TL, Dubrovsky JG (2008) Determinate root growth and meristem maintenance in angiosperms. Ann Bot 101(3):319–340

    Article  CAS  PubMed  Google Scholar 

  • Smith S, De Smet I (2012) Root system architecture: insights from Arabidopsis and cereal crops. Philos Trans R Soc Lond B Biol Sci 367:1441–1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solans M, Messuti MI, Reiner G, Boenel M, Vobis G, Wall LG, Scervino JM (2019) Exploring the response of Actinobacteria to the presence of phosphorus salts sources: Metabolic and co-metabolic processes. J Basic Microbiol 59:487–495

    Article  CAS  PubMed  Google Scholar 

  • Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3:a001438

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J (2014) Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol 201:850–861

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18:607–621

    Article  CAS  PubMed  Google Scholar 

  • Tzec-Interián JA, Desgarennes D, Carrión G, Monribot-Villanueva JL, Guerrero-Analco JA, Ferrera-Rodríguez O, Santos-Rodríguez DL, Liahut-Guin N, Caballero-Reyes GE, Ortiz-Castro R (2020) Characterization of plant growth-promoting bacteria associated with avocado trees (Persea americana Miller) and their potential use in the biocontrol of Scirtothrips perseae (avocado thrips). PloS One 15(4):e0231215

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reported genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136(6):1005–1016

    Article  CAS  PubMed  Google Scholar 

  • Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 162:304–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou F, Emonet A, Dénervaud Tendon V, Marhavy P, Wu D, Lahaye T, Geldner N (2020) Co-incidence of damage and microbial patterns controls localized immune responses in roots. Cell 180(3):440-453.e18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank to Drs. Ben Scheres, Alfredo Cruz Ramirez, and Mark Estelle for donation of Arabidopsis transgenic and mutant lines, and Ofelia Ferrera Rodríguez and Greta Hanako Rosas Saito for support in microscopy and molecular analysis.

Funding

This work was founded by grants from SEP-CONACYT A1-S-34768.

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Authors and Affiliations

  1. Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Edificio B3, Ciudad Universitaria, C. P. 58030, Morelia, Michoacán, México

    Elizabeth García-Cárdenas, León Francisco Ruiz-Herrera, Eduardo Valencia-Cantero & José López-Bucio

  2. Catedrático CONACYT-Instituto de Ecología A.C. Red de Estudios Moleculares Avanzados, Clúster BioMimic®, Instituto de Ecología A.C. Carretera Antigua a Coatepec, 351, El Haya, Xalapa, Veracruz, 91073, México

    Randy Ortiz-Castro

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  1. Elizabeth García-Cárdenas
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  4. Eduardo Valencia-Cantero
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Contributions

E.G.C., R.O.C., L.F.R.H., and E.V.C. performed the experiments. E.G.C., R.O.C., L.F.R.H., E.V.C., and J.L.B. analyzed the data. E.G.C. and J.L.B. designed the experiments and wrote the manuscript. J.L.B. applied for funding. All authors approved the manuscript.

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Correspondence to José López-Bucio.

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García-Cárdenas, E., Ortiz-Castro, R., Ruiz-Herrera, L.F. et al. Micrococcus luteus LS570 promotes root branching in Arabidopsis via decreasing apical dominance of the primary root and an enhanced auxin response. Protoplasma 259, 1139–1155 (2022). https://doi.org/10.1007/s00709-021-01724-z

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