Agave Seed Endophytes: Ecology and Impacts on Root Architecture, Nutrient Acquisition, and Cold Stress Tolerance

  • America Martinez-Rodriguez
  • Gloria Macedo-Raygoza
  • Aurora X. Huerta-Robles
  • Ileana Reyes-Sepulveda
  • Jhovana Lozano-Lopez
  • Evelyn Y. García-Ochoa
  • Luis Fierro-Kong
  • Marisa H. G. Medeiros
  • Paolo Di Mascio
  • James Francis WhiteJr
  • Miguel J. Beltran-Garcia


The genus Agave comprises plants that are a source of nutrients for humans and animals and can support their ecosystems. Agave extinction may impact a long list of organisms including plants, pollinators, animals, and soil microorganisms. Agaves have an extraordinary adaptability to arid and semiarid environments. Physiological and morphological strategies allow them to survive under extreme conditions such as drought and high temperature (up to 61 °C). In recent decades it has been discovered that bacterial and fungal communities in plants are not simple passengers, and this is especially true for microbial communities of seeds. Seed transmission of endophytic microbes appears to be important in shaping the endophyte community in the mature plant and consequently acts as the initial inoculum for the plant microbiota. Those microbes participate in seedling growth, favor intake of nutrients and resistance to abiotic and biotic stress, and, in some extreme cases, can be used as “food” for the plants.


Agave angustifolia Agave tequilana Agave marmorata Bacillus tequilensis Chilling stress Endophytes Enterobacter MALDI-IMS Metabolomics Nutrient acquisition Pseudomonas aeruginosa Root architecture Root hairs ROS 



The Mexican group gratefully acknowledges the financial support from CONACYT: Proyectos de Desarrollo Cientifico para atender Problemas Nacionales (CONACYT 212875); Project 207400 of Bilateral Cooperation Mexico-Brazil funded by CONACYT and CNPq (Brazil, No. 490440/2013-4); Apoyo al fortalecimiento y desarrollo de la infraestructura científica y tecnológica convocatoria 2016-269607. A.M-R G.M-R and A.H-R thanks CONACYT for PhD fellowships # 720754, #256660 and #414739 respectively. Paolo Di Mascio thanks PFAPESP (Funda. o de Amparo. Pesquisa do Estado de Sao Paulo, No. 2012/12663-1, CEPID Redoxoma No. 2013/07937-8), CNPq (Conselho Nacional para o Desenvolvimento Científico e Tecnológico, No. 301307/2013-0, No. 159068/2014-2). Marisa H.G. Medeiros No. 159068/2014-2), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), PRPUSP (Pro-Reitoria de Pesquisa da Universidade de São Paulo, NAP Redoxoma no. 2011.1.9352.1.8) and John Simon Guggenheim Memorial Foundation (P.D.M. Fellowship) for financial support. James Francis White is also grateful for support from USDA-NIFA Multistate Project W3157 and the New Jersey Agricultural Experiment Station. This book chapter is dedicated to the memory of my wife Dr. Cecilia Vélez-Gutierréz, who recently passed away (15/01/2019). Thank you for your courage, discussions and teachings as well as motivating me to approach agaves as a model for endophyte studies, I will always love you.


  1. Abraham P, Yin H, Borland A, Weighill D, Lim SD et al (2016) Transcript, protein and metabolite temporal dynamics in the CAM plant Agave. Nat Plants 2:16178. Scholar
  2. Abraham-Juárez M, Hernández-Cárdenas R, Santoyo-Villa J, O’Connor D, Sluis A, Hake S, Ordaz-Ortiz J, Terry L, Simpson J (2015) Functionally different PIN proteins control auxin flux during bullbin development in Agave tequilana. J Exp Bot 66(13):3893–3905. Scholar
  3. Abreu E, Aragão F (2007) Isolation and characterization of a myo-inositol-1-phosphate synthase gene from yellow passion fruit (Passiflora edulis f. flavicarpa) expressed during seed development and environmental stress. Ann Bot 99:285–292. Scholar
  4. Alavi P, Müller H, Cardinale M, Zachow C, Sánchez M, Martínez J, Berg G (2013) The DSF quorum sensing system controls the positive influence of Stenotrophomonas maltophilia on plants. PLoS One 8(7):e67103. Scholar
  5. Almaguer C, Cheng W, Nolder C, Vogt P (2004) Glycerophosphoinositol, a novel phosphate source whose transport is regulated by multiple factors in Saccharomyces cerevisiae. J Biol Chem 279(30):31937–31942. Scholar
  6. Aquino-Bolaños T, Ruiz-Vega J, Giron-Pablo S, Pérez-Pacheco R, Martínez-Tomas S, Silva-Rivera M (2011) Interrelationships of the agave weevil Scyphophorus acupunctatus (Gyllenhal), Erwinia carotovora (Dye), entomopathogenic agents and agrochemicals. Afr J Biotechnol 10(68):15402–15406. Scholar
  7. Arizaga S, Ezcurra E (1995) Insurance against reproductive failure in a semelparous plant: bulbil formation in Agave macroacantha flowering stalks. Oecologia 101:329–334. Scholar
  8. Arizaga S, Ezcurra E (2002) Propagation mechanisms in Agave macroacantha (Agavaceae), a tropical arid-land succulent rosette. Am J Bot 89(4):632–641.1.
  9. Banskar S, Mourya D, Shouche Y (2016a) Bacterial diversity indicates dietary overlap among bats of different feeding habits. Microbiol Res 182:99–108. Scholar
  10. Banskar S, Bhute S, Suryavanshi M, Punekar S, Shouche Y (2016b) Microbiome analysis reveals the abundance of bacterial pathogens in Rousettus leschenaultii guano. Sci Rep 6:36948. Scholar
  11. Barret M, Briand M, Bonneau S, Préveaux A, Valiere S, Bouchez O, Hunault G, Simoneau P, Jacques M (2015) Emergence shapes the structure of the seed microbiota. Appl Environ Microbiol 81(4):1256–1266. Scholar
  12. Barret M, Guimbaud J, Darrasse A, Jacques M (2016) Plant microbiota affects seed transmission of phytopathogenic micro-organisms. Mol Plant Pathol 17:791–795. Scholar
  13. Behie S, Zelisko P, Bidochka M (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336(6088):1576–1577. Scholar
  14. Beltran-Garcia M, White J, Prado F, Prieto K, Yamaguchi L, Torres M, Kato M, Medeiros M, Di Mascio P (2014) Nitrogen acquisition in Agave tequilana from degradation of endophytic bacteria. Sci Rep 6(4):6938. Scholar
  15. Borbón-Palomares D, Laborin-Sirivirian F, Tinoco-Ojanguren C, Peñalba M, Reyes-Ortega I, Molina-Freaner F (2018) Reproductive ecology of Agave colorata: the importance of nectar-feeding bats and the germination consequences of self-pollination. Plant Ecol 219:927–939. Scholar
  16. Campos H, Trejo C, Peña-Valdivia C, García-Nava R, Conde-Martínez V, Cruz-Ortega M (2014) Photosynthetic acclimation to drought stress in Agave salmiana otto ex Salm-Dyck seedlings is largely dependent on thermal dissipation and enhanced electron flux to photosystem I. Photosynth Res 122(1):23–39. Scholar
  17. Carrillo-Araujo M, Tas N, Alcántara-Hernández R, Gaona O, Schondube J, Medellín R, Jansson J, Falcón L (2015) Phyllostomid bat microbiome composition is associated to host phylogeny and feeding strategies. Front Microbiol 6:447. Scholar
  18. Carvalho T, Ballesteros H, Thiebaut F, Ferreira P, Hemrly A (2016) Nice to meet you: genetic, epigenetic and metabolic controls of plant perception of beneficial associative and endophytic diazotrophic bacteria in non-leguminous plants. Plant Mol Biol 90:561–574. Scholar
  19. Chen N, He R, Chai Q, Li C, Nan Z (2016) Transcriptomic analyses giving insights into molecular regulation mechanisms involved in cold tolerance by Epichloë endophyte in seed germination of Achnatherum inebrians. Plant Growth Regul 80(3):367–375. Scholar
  20. Chen H, Wu H, Yan B, Zhao H, Liu F, Zhang H, Sheng Q, Miao F, Liang Z (2018) Core microbiome of medicinal plant Salvia miltiorrhiza seed: a rich reservoir of beneficial microbes for secondary metabolism? Int J Mol Sci 19:672. Scholar
  21. Coleman-Derr D, Desgarennes D, Fonseca-Garcia C et al (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209(2):798–811. Scholar
  22. Cuevas-Juárez E, Ávila-Fernández Á, López-Munguía A (2017) Identification of enzymatic activities involved in agave fructan consumption by Bifidobacterium longum subsp. infantis ATCC 15697. J Funt Foods 35:267–278. Scholar
  23. Desgarennes D, Garrido E, Torres-Gomez M, Peña-Cabriales J, Partida-Matinez L (2014) Diazotrophic potential among bacterial communities associated with wild and cultivated Agave species. FEMS Microbiol Ecol 90:844–857. Scholar
  24. Dutilleul C, Chavarria H, Rézé N, Sotta B, Baudouin E, Guillas I (2015) Evidence for ACD5 ceramide kinase activity involvement in Arabidopsis response to cold stress. Plant Cell Environ 38:2688–2697. Scholar
  25. Edwards J, Johnson C, Santos-Medellón C, Lurie E, Kumar-Podishetty N, Chatnagar S, Eisen J, Venkatesan-Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112:E911–E920. Scholar
  26. Escalante A, Lopez-Soto D, Velázquez-Gutiérrez J, Giles-Gómez M, Bolibar F, López-Munguía A (2016) Pulque, a traditional Mexican alcoholic fermented beverage: historical, microbiological, and technical aspects. Front Microbiol 7:1026. Scholar
  27. Escobar-Guzmán R, Zamudio-Hernández F, Gil-Vega K, Simpson J (2008) Seed production and gametophyte formation in Agave tequilana and Agave americana. Botany 86:1343–1353. Scholar
  28. Fonseca-García C, Desgarennes D, Flores-Núñez V, Partida-Martínez L (2018) The microbiome of desert cam plants: lessons from amplicon sequencing and metagenomics. In: Nagarajan M (ed) Metagenomics: perspectives, methods, and applications. Elsevier, Amsterdam, pp 213–254. ISBN: 978-0-08-102268-9.
  29. Fonseca-Sepulveda C (2017) Identification of bacteria associated with the soft-rot of Agave tequilana and endophytic bacteria obtained from healthy by mass spectrometry MALDI-TOF. BSc Thesis, Universidad Autónomas de Guadalajara, 17 June 2017Google Scholar
  30. Franco-Robles E, López M (2016) Agavins increase neurotrophic factors and decrease oxidative stress in the brains of high-fat diet-induced obese mice. Molecules 21(8):e998. Scholar
  31. Galicia M, Buenrostro A, García J (2014) Specific bacterial diversity in bats of different food guilds in Southern sierra Oaxaca. Mexico Rev Biol Trop 62(4):1673–1681CrossRefGoogle Scholar
  32. García-Mendoza AJ (2011) Agavaceae. Flora del Valle de Tehuacán Cuicatlán. Instituto de Biología, Universidad Nacional Autónoma de México yComisión Nacional para el Conocimiento y Uso de la Biodiversidad, México. ISBN: 978-607-02-2566-6.Google Scholar
  33. Giles-Gómez M, Sandoval-García J, Matus V, Campos-Quintana I, Bolívar F, Escalante A (2016) In vitro and in vivo probiotics assessment of Leuconostoc mesenteroides P45 isolated from pulque, a Mexican traditional alcoholic beverage. Springerplus 5(1):708. Scholar
  34. Good-Avila S, Souza V, Gaut B, Equiarte L (2006) Timing and rate of speciation in Agave (Agavaceae). Proc Natl Acad Sci USA 103:9124–9129. Scholar
  35. Hou Q, Ufer G, Bartels D (2016) Lipid signalling in plant responses to abiotic stress. Plant Cell Environ 39:1029–1048. Scholar
  36. Huanzano-García A, López M (2018) Enzymatic hydrolysis of agavins to generate branched fructooligosaccharides (a-FOS). Appl Biochem Biotechnol 184(1):25–34. Scholar
  37. Huerta-Lovera M, Peña-Valdivia C, García-Esteva A et al (2018) Maguey (Agave salmiana) infructescence morphology and its relationship to yield components. Genet Resour Crop Evol 65:1649–1661. Scholar
  38. Irizarry I, White JF (2018) Bacillus amyloliquefaciens alters gene expression, ROS production and lignin synthesis in cotton seedling roots. J Appl Microbiol 124(6):1589–1603CrossRefGoogle Scholar
  39. Janmohammadi M (2012) Metabolomic analysis of low temperature responses in plants. Curr Opin Agric 1(1):1–6Google Scholar
  40. Johnston-Monje D, Raizada M (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6(6):e20396. Scholar
  41. Kakar K, Nawaz Z, Cui Z, Almoneafy A, Ullah R, Shu Q (2018) Rhizosphere-associated Alcaligenes and Bacillus strains that induce resistance against blast and sheath blight diseases, enhance plant growth and improve mineral content in rice. J Appl Microbiol 124(3):779–796. Scholar
  42. Kaspar S, Peukert M, Stavos A, Matros A, Mock H (2011) MALDI-imaging mass spectrometry – an emerging technique in plant biology. Proteomics 11:1840–1850. Scholar
  43. Khalaf E, Raizada M (2016) Taxonomic and functional diversity of cultured seed associated microbes of the cucurbit family. BMC Microbiol 16:131. Scholar
  44. Krol A, Amarowicz R, Weidner S (2015) The effects of cold stress on the phenolic compounds and antioxidant capacity of grapevine (Vitis vinifera L.) leaves. J Plant Physiol 15(189):97–104. Scholar
  45. Li S, Yang Y, Zhang Q, Ningfang L, Xu Q, Hu L (2018) Differential physiological and metabolic response to low temperature in two zoysiagrass genotypes native to high and low latitude. PLoS One 13(6):E0198885. Scholar
  46. Liu Y, Zuo S, Zou Y, Wang J, Song W (2013) Investigation on diversity and population succession dynamics of endophytic bacteria from seeds of maize (Zea mays L., Nongda108) at different growth stages. Ann Microbiol 63:71–79. Scholar
  47. Lonhienne T, Mason MG, Ragan MA, Hugenholtz P, Schmidt S, Paungfoo-Lonhienne C (2014) Yeast as a biofertilizer alters plant growth and morphology. Crop Sci 54:785–790. Scholar
  48. Lopez B, Bashan Y, Bacolio M (2011) Endophytic bacteria of Mammillaria fraileana, an endemic rock-colonizing cactus of the southern Sonoran Desert. Arch Microbiol 193:527–541. Scholar
  49. López-Bucio J, Campos-Cuevas J, Henández-Calderón E, Velásquez-Becerra C, Faría-Rodríguez R, Macías-Rodríguez L, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20(2):207–217. Scholar
  50. Lundberg D, Lebeis S, Herrera-Paredes S, Yourstone S, Gehring J, Malfarri S, Tremblay J, Engelbrektson A, Kunin V, Glavina del Río T, Edgar R, Eickhorst T, Ley R, Hugenholtz P, Green-Tringe S, Dangl J (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90. Scholar
  51. Martínez-Rodríguez J, Mora-Amutio M, Plascencia-Correa L et al (2014) Cultivable endophytic bacteria from leaf bases of Agave tequilana and their role as plant growth promoters. Braz J Microbiol 45(4):1333–1339. Scholar
  52. Matiz A, Mioto P, Mayorga A, Freschi L, Mercier H (2013) CAM photosynthesis in bromeliads and agaves: what can we learn from these plants? In: Dubinsky Z (ed) Photosynthesis. InTech. ISBN: 978-953-51-1161-0.
  53. Michaelson LV, Napier JA, Molino D, Faure J-D (2016) Plant sphingolipids: their importance in cellular organization and adaption. Biochim Biophys Acta 1861(9):1329–1335CrossRefGoogle Scholar
  54. Monja-Mio K, Barredo Pool F, Herrera-Herrera G, Esqueda-Valle M, Robert M (2015) Development of the stomatal complex and leaf Surface of Agave angustifolia Haw. ‘Bacanora’ plantlets during in vitro to ex vitro transition process. Sci Hortic 189:32–40. Scholar
  55. Nava-Cruz N, Medina-Morales A, Martinez J, Rodriguez R, Aguilar C (2015) Agave biotechnology: an overview. Crit Rev Biotechnol 35(4):546–559. Scholar
  56. Nelson EB (2018) The seed microbiome: origins, interactions, and impacts. Plant and Soil 422:7–34. Scholar
  57. Ornelas J, Ordano M, Hernandez A, Lopez J, Mendoza L, Perroni Y (2002) Nectar oasis produced by Agave marmorata Roezl. (Agavaceae) lead to spatial and temporal segregation among nectarivores in the Tehuacan Valley, Mexico. J Arid Environ 52:37–51. Scholar
  58. Parada A, Rodrigues V, Nogueira E, Labanca E, Preira M (2016) Nitrogen metabolism and growth of wheat plant under diazotrophic endophytic bacteria inoculation. Appl Soil Ecol 107:313–319. Scholar
  59. Pastore D, Trono D, Laus MN, Di Fonzo N, Flagella Z (2007) Possible plant mitochondria involvement in cell adaptation to drought stress. A case study: durum wheat mitochondria. J Exp Bot 58:195–210. Scholar
  60. Paungfoo-Lonhienne C, Rentsch D, Robatzek S, Webb RI, Sagulenko E, Näsholm T, Schmidt S, Lonhienne TGA, Kroymann J (2010) Turning the table: plants consume microbes as a source of nutrients. PLoS ONE 5(7):e11915CrossRefGoogle Scholar
  61. Pitzschle A (2018) Molecular dynamics in germinating, endophyte-colonized quinoa seeds. Plant Soil 422:135–154. Scholar
  62. Popov V, Purvis A, Skulachev V, Wagner A (2001) Stress-induced changes in ubiquinone concentration and alternative oxidase in plant mitochondria. Biosci Rep 21(3):369–379CrossRefGoogle Scholar
  63. Prieto K, Echaide-Aquino F, Huerta Robles A, Valérino H, Macedo-Raygoza G, Prado F, Medeiros M, Brito H, da Silva I, Cunha-Felinto M, White Jr J, Di Mascio P, Beltran-Garcia M (2017) Endophytic bacteria and rare earth elements; promising candidates for nutrient use efficiency in plants. In: Anwa M (ed) Plant macronutrient use efficiency. Academic, Cambridge, pp 285–306. ISBN: 978-0-12-811308-0.
  64. Puente M, Ching L, Bashan Y (2009) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408. Scholar
  65. Raheem A, Shaposhnikov A, Belimov A, Dodd I, Ali B (2018) Auxin production by rhizobacteria was associated with improved yield of wheat (Triticum aestivum L.) under drought stress. Arch Agro Soil Sci 64(4):574–587. Scholar
  66. Rahman MM, Flory E, Werner H, Abideen Z, Schikora A, Surez C, Schnell S, Cardinale M (2018) Consistent associations with beneficial bacteria in the seed endosphere of barley (Hordeum vulgare L.). Syst Appl Microbiol 41(4):386–398. Scholar
  67. Ramírez-Ramírez M, Mancilla-Margalli N, Meza-Álvarez L, Turincio-Tadeo R, Guzmán-de Pena D, Avila-Miranda (2017) Epidemiology of Fusarium agave wilt in Agave tequilana WEBER var. Azul. Plant Prot Sci 53:144–152. Scholar
  68. Redman R, Kim Y, Woodward C, Greer C, Espino L, Doty S, Rodriguez R (2011) Increased fitness of rise plant to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6(7):e:14823. Scholar
  69. Rybakova D, Mancinelli R, Wikström M, Birch-Jensen A, Postma J, Ehlers R, Goertz S, Berg G (2017) The structure of the Brassica napus seed microbiome is cultivar-dependent and affects the interactions of symbionts and pathogens. Microbiome 5:104. Scholar
  70. Shade A, Handelsman J (2012) Beyond the venn diagram: the hunt for a core microbiome. Environ Microbiol 14(1):4–12. Scholar
  71. Shade A, Jacques M, Barret M (2017) Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr Opin Microbiol 37:15–22. Scholar
  72. Shahzad R, Khan A, Bibal S, Asaf S, Lee I (2018) What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Front Plant Sci 9:24. Scholar
  73. Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21:3823–3838. Scholar
  74. Singh RP, Jha PN (2017) The PGPR Stenotrophomonas maltophilia SBP-9 augments resistance against biotic and abiotic stress in wheat plants. Front Microbiol 8:1945.
  75. Sinha S, Kukreja B, Arora P, Sharma M, Pandey G, Agarwal M, Chinnusamy V (2015) The omics of cold stress responses in plants. In: Pandey G (ed) Elucidation of abiotic stress signaling in plants. Springer, New York, pp 143–194. Scholar
  76. Slauson LA (2000) Pollination biology of two chiropterophilous agaves in Arizona. Am J Bot 87(6):825–836. Scholar
  77. Stewart JR (2015) Agave as model CAM crop system for a warming and warming and drying world. Front Plant Sci 6:684–707. Scholar
  78. Steyn W, Wand S, Holcroft D, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed united function in photoprotection. New Phytol 155(3):349–361CrossRefGoogle Scholar
  79. Sukumar P, Legué V, Vayssiéres A, Martin F, Tuskan G, Kalluri U (2013) Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions. Plant Cell Environ 36:909–919. Scholar
  80. Torres-Cortés G, Bonneau S, Bouchez O, Genthon C, Briand M, Jacques M, Barret M (2018) Functional microbial features driving community assembly during seed germination and emergence. Front Plant Sci 9:902. Scholar
  81. Trejo-Salazar R, Scheinvar E, Eguiarte L (2015) ¿Quién poliniza realmente los agaves? Diversidad de visitantes florales en 3 especies de Agave (Agavoideae: Asparagaceae). Rev Mex Bio 86:358–369. Scholar
  82. Trejo-Salazar R, Eguiarte L, Suro-Piñera D, Medellin R (2016) Save our bats, save our tequila: industry and science join forces to help bats and Agaves. Nat Areas J 36(5):523–530. Scholar
  83. Truyens S, Weyens N, Cuypers A, Vangronsveld J (2014) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7:40–50. Scholar
  84. Vega-Ramos K, Uvalle-Bueno J, Gómez-Leyva J (2013) Molecular variability among isolates of Fusarium oxysporum associated with root rot disease of Agave tequilana. Biochem Genet 51:243–255. Scholar
  85. Velickovic D, Anderton C (2017) Mass spectrometry imaging: towards mapping the elemental and molecular composition of the rhizosphere. Rhizosphere 3:254–258. Scholar
  86. Verma SK, Kingsley K, Irizarry I, Bergen M, Kharwar R, White J Jr (2017) Seed vectored endophytic bacteria modulate development of rice seedlings. J Appl Microbiol 122:1680–1691. Scholar
  87. Wright I, Dong N, Maire V, Coli-Prentice I et al (2017) Global climatic drivers of leaf size. Science 357(6354):917–921. Scholar
  88. White JF, Crawford H, Torres MS, Mattera R, Irizarry I, Bergen M (2012) A proposed mechanism for nitrogen acquisition by grass seedlings through oxidation of symbiotic bacteria. Symbiosis 57:161–171CrossRefGoogle Scholar
  89. White JF, Torres MS, Somu MP, Johnson H, Irizarry I, Chen Q, Zhang N, Walsh E, Tadych M, Bergen M (2014) Hydrogen peroxide staining to visualize intracellular bacterial infections of seedling root cells. Microsc Res Tech 77:566–573CrossRefGoogle Scholar
  90. White JF, Kingsley K, Kowalski K, Irizarry I, Micci A, Soares M, Bergen M (2018) Disease protection and allelopathic interactions of seed-transmitted endophytic Pseudomonads of invasive reed grass (Phragmites australis). Plant Soil 422:195–208. Scholar
  91. Yang L, Danzberger J, Schöler A, Schöler P, Schloter M, Radl V (2017) Dominant groups of potentially active bacteria shared by barley seeds become less abundant in root associated microbiome. Front Plant Sci 8:1005. Scholar
  92. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse C (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 162:304–318. Scholar
  93. Zhang J, Zhang C, Yang J, Zhang R, Gao J, Zhao X, Zhao J, Zhao D, Zhang X (2018) Insights into endophytic bacterial community structures of seeds among various Oryza sativa L. rice genotypes. J Plant Growth Regul 1–10.
  94. Zhou Y, Zeng L, Fu X, Mei X, Cheng S, Liao Y, Deng R, Xu X, Jiang Y, Duan X, Baldermann S, Yang Z (2016) The sphingolipid biosynthetic enzyme Sphingolipid delta8 desaturase is important for chilling resistance of tomato. Sci Rep 6:38742. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • America Martinez-Rodriguez
    • 1
  • Gloria Macedo-Raygoza
    • 2
  • Aurora X. Huerta-Robles
    • 1
  • Ileana Reyes-Sepulveda
    • 2
  • Jhovana Lozano-Lopez
    • 2
  • Evelyn Y. García-Ochoa
    • 2
  • Luis Fierro-Kong
    • 2
  • Marisa H. G. Medeiros
    • 3
  • Paolo Di Mascio
    • 3
  • James Francis WhiteJr
    • 4
  • Miguel J. Beltran-Garcia
    • 2
  1. 1.Institute of EngineeringUniversidad Autónoma de Baja CaliforniaMexicaliMéxico
  2. 2.Department of Chemistry-E-BuildingUniversidad Autonoma de GuadalajaraZapopanMexico
  3. 3.Department of Biochemistry, Institute of ChemistryUniversidade de Sao PauloSão PauloBrazil
  4. 4.Department of Plant BiologyRutgers UniversityNew BrunswickUSA

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