2,023
Views
0
CrossRef citations to date
0
Altmetric
Plant-Microorganism Interactions

The endophyte’s endophytes: the microbial partners of the endangered plant parasite Rafflesia speciosa (Rafflesiaceae) reveal clues about its cryptic biology and cues for cultivation

ORCID Icon, , , , , , , , , , , , , , , , , , , , , , , & show all
Article: 2304221 | Received 25 Sep 2023, Accepted 07 Jan 2024, Published online: 20 Jan 2024

References

  • Afzal I, Shinwari ZK, Sikandar S, Shahzad S. 2019. Plant beneficial endophytic bacteria: mechanisms, diversity, host range and genetic determinants. Microbiol Res. 221:36–49. doi:10.1016/j.micres.2019.02.001.
  • Agrios GN. 2005. Plant pathology, Fifth Edition. Burlington, MA: Elsevier Academic Press.
  • Aguilar-Marcelino L, Mendoza-de-Gives P, Al-Ani LKT, López-Arellano ME, Gómez-Rodríguez O, Villar-Luna E, Reyes-Guerrero DE. 2020. Using molecular techniques applied to beneficial microorganisms as biotechnological tools for controlling agricultural plant pathogens and pest. pages 333-349 in: molecular aspects of plant beneficial microbes in agriculture. Elsevier.
  • Ambika Manirajan B, Ratering S, Rusch V, Schwiertz A, Geissler-Plaum R, Cardinale M, Schnell S. 2016. Bacterial microbiota associated with flower pollen is influenced by pollination type, and shows a high degree of diversity and species-specificity. Environ Microbiol. 18:5161–5174. doi:10.1111/1462-2920.13524.
  • Angus AA, Agapakis CM, Fong S, Yerrapragada S, Estrada-de Los Santos P, Yang P, Song N, Kano S, Caballero-Mellado J, De Faria SM. 2014. Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. PLoS One. 9:e83779. doi:10.1371/journal.pone.0083779.
  • Barron, G. L. 2004. Fungal parasites and predators of rotifers, nematodes, and other invertebrates, 435-450 in: Biodiversity of fungi, inventory and monitoring methods. G. M. Muller, Bills G., Foster, M.S, ed. Elsevier Academic Press, Amsterdam.
  • Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F. 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 37:852–857. doi:10.1038/s41587-019-0209-9.
  • Bouman F, Meijer W. 1994. Comparative structure of ovules and seeds inRafflesiaceae. Plant Syst Evol. 193:187–212. doi:10.1007/BF00983550.
  • Boutard M, Cerisy T, Nogue P-Y, Alberti A, Weissenbach J, Salanoubat M, Tolonen AC. 2014. Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass. PLoS Genet. 10:e1004773. doi:10.1371/journal.pgen.1004773.
  • Bridges CM, Gage DJ. 2021. Development and application of aerobic, chemically defined media for Dysgonomonas. Anaerobe. 67:102302. doi:10.1016/j.anaerobe.2020.102302.
  • Cai L, Arnold BJ, Xi Z, Khost DE, Patel N, Hartmann CB, Manickam S, Sasirat S, Nikolov LA, Mathews S, et al. 2021. Deeply altered genome architecture in the endoparasitic flowering plant Sapria himalayana Griff. (Rafflesiaceae). Curr Biol. 31:1002–1011.
  • Castillo Lopez D, Zhu-Salzman K, Ek-Ramos MJ, Sword GA. 2014. The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS One. 9:e103891. doi:10.1371/journal.pone.0103891.
  • Chen P, Chen L, Wen J. 2011. The first phylogenetic analysis of Tetrastigma(Miq.) Planch., the host of Rafflesiaceae. Taxon. 60:499–512. doi:10.1002/tax.602017.
  • Chen Y, Liao K, Ai L, Guo P, Huang H, Wu Z, Liu M. 2017. Risk factors, perceptions and practices associated with taenia solium cysticercosis and its control in the smallholder pig production systems in Uganda: a cross-sectional survey. BMC Infect Dis. 17:1–4. doi:10.1186/s12879-016-2122-x.
  • Davis CC. 2008. Floral evolution: dramatic size change was recent and rapid in the world's largest flowers. Curr Biol. 18:R1102–R1104.
  • Duar RM, Lin XB, Zheng J, Martino ME, Grenier T, Pérez-Muñoz ME, Leulier F, Gänzle M, Walter J. 2017. Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS microbiology reviews 41:S27-S48.
  • Duda VI, Suzina NE, Esikova TZ, Akimov VN, Oleinikov RR, Oleinikov RR, Polivtseva VN, Abashina TN, Shorokhova AP, Boronin AM. 2009. A cytological characterization of the parasitic action of ultramicrobacteria NF1 and NF3 of the genus Kaistia on chemoorganotrophic and phototrophic bacteria. FEMS Microbiol Ecol. 69:180–193. doi:10.1111/j.1574-6941.2009.00696.x.
  • Durlik K, Żarnowiec P, Piwowarczyk R, Kaca W. 2021. Culturable endophytic bacteria fromPhelipanche ramosa(Orobanchaceae) seeds. Seed Sci Res. 31:69–75. doi:10.1017/S0960258520000343.
  • Effantin G, Rivasseau C, Gromova M, Bligny R, Hugouvieux-Cotte-Pattat N. 2011. Massive production of butanediol during plant infection by phytopathogenic bacteria of the genera Dickeya and Pectobacterium. Mol Microbiol. 82:988–997. doi:10.1111/j.1365-2958.2011.07881.x.
  • Eid AM, Fouda A, Abdel-Rahman MA, Salem SS, Elsaied A, Oelmüller R, Hijri M, Bhowmik A, Elkelish A, Hassan SE-D. 2021. Harnessing bacterial endophytes for promotion of plant growth and biotechnological applications: an overview. Plants. 10:935. doi:10.3390/plants10050935.
  • Evseev P, Lukianova A, Tarakanov R, Tokmakova A, Shneider M, Ignatov A, Miroshnikov K. 2022. Curtobacterium spp. and Curtobacterium flaccumfaciens: phylogeny, genomics-based taxonomy, pathogenicity, and diagnostics. Curr Issues Mol Biol. 44:889–927. doi:10.3390/cimb44020060.
  • Felestrino ÉB, Santiago IF, Freitas L, Rosa LH, Ribeiro SP, Moreira LM. 2017. Plant growth promoting bacteria associated with langsdorffia hypogaea-rhizosphere-host biological interface: a neglected model of bacterial prospection. Front Microbiol. 08:172. doi:10.3389/fmicb.2017.00172.
  • Figueiredo GGO, Lopes VR, Romano T, Camara MC. 2020. Clostridium. In: N. Amaresan, M. S. Kumar, K. K. K. Annapurna, A. Sankaranarayanan, editor. Beneficial microbes in agro-ecology: bacteria and fungi. eds. Cambridge, MA, USA: Academic Press; p. 477–491.
  • Fitzpatrick CR, Schneider AC. 2020. Unique bacterial assembly, composition, and interactions in a parasitic plant and its host. J Exp Bot. 71:2198–2209. doi:10.1093/jxb/erz572.
  • Fondevilla S, Fernández-Aparicio M, Satovic Z, et al. 2010. Identification of quantitative trait loci for specific mechanisms of resistance to Orobanche crenata Forsk. in pea (Pisum sativum L.). Mol Breed. 25:259–272. doi:10.1007/s11032-009-9330-7.
  • García-Cárdenas E, Ortiz-Castro R, Ruiz-Herrera LF, Valencia-Cantero E, López- Bucio J. 2022. 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. doi:10.1007/s00709-021-01724-z.
  • Giovannini L, Palla M, Agnolucci M, Avio L, Sbrana C, Turrini A, Giovannetti M. 2020. Arbuscular mycorrhizal fungi and associated microbiota as plant biostimulants: research strategies for the selection of the best performing inocula. Agronomy. 10:106. doi:10.3390/agronomy10010106.
  • Gómez-Godínez LJ, Aguirre-Noyola JL, Martínez-Romero E, Arteaga-Garibay RI, Ireta- Moreno J, Ruvalcaba-Gómez JM. 2023. A look at plant-growth-promoting bacteria. Plants. 12:1668. doi:10.3390/plants12081668.
  • Hawar SN. 2022. Extracellular enzyme of endophytic fungi isolated from Ziziphus spina leaves as medicinal plant. Int J Biomater.
  • He Y, Xie Z, Zhang H, Liebl W, Toyama H, Chen F. 2022. Oxidative fermentation of acetic acid bacteria and its products. Front Microbiol. 13:879246. doi:10.3389/fmicb.2022.879246.
  • Iasur Kruh L, Lahav T, Abu-Nassar J, Achdari G, Salami R, Freilich S, Aly R. 2017. Host-parasite-bacteria triangle: the microbiome of the parasitic weed phelipanche aegyptiaca and tomato-solanum lycopersicum (mill.) as a host. Front Plant Sci. 8:269. doi:10.3389/fpls.2017.00269.
  • Jaffar NS, Jawan R, Chong KP. 2023. The potential of lactic acid bacteria in mediating the control of plant diseases and plant growth stimulation in crop production - A mini review. Front Plant Sci. 13:1047945. doi:10.3389/fpls.2022.1047945.
  • Janusz G, Pawlik A, Sulej J, Świderska-Burek U, Jarosz-Wilkołazka A, Paszczyński A. 2017. Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol Rev. 41:941–962. doi:10.1093/femsre/fux049.
  • Jing M, Xu X, Peng J, Li C, Zhang H, Lian C, Chen Y, Shen Z, Chen C. 2022. Comparative genomics of three Aspergillus strains reveals insights into endophytic lifestyle and endophyte-induced plant growth promotion. Journal of Fungi. 8:690. doi:10.3390/jof8070690.
  • Kandel SL, Joubert PM, Doty SL. 2017. Bacterial endophyte colonization and distribution within plants. Microorganisms. 5:77. doi:10.3390/microorganisms5040077.
  • Kawa D, Thiombiano B, Shimels M, Taylor T, Walmsley A, Vahldick HE, Leite M, Musa Z, Bucksch A, Dini-Andreote F, et al. 2022. The soil microbiome reduces Striga infection of sorghum by modulation of host-derived signaling molecules and root development. bioRxiv. doi:10.1101/2022.11.06.515382.
  • Khalaf EM, Raizada MN. 2016. Contributions of tropodithietic acid and biofilm formation to the probiotic activity of Phaeobacter inhibens. BMC Microbiol. 16:1–16. doi:10.1186/s12866-015-0617-z.
  • Kim S-J, Lim J-M, Ahn J-H, Weon H-Y, Hamada M, Suzuki K-i, Ahn T-Y, Kwon S-W. 2014. Description of Galbitalea soli gen. nov., sp. nov., and Frondihabitans Sucicola sp. nov. Int J Syst Evol Microbiol. 64:572–578.
  • Lagkouvardos I, Lesker TR, Hitch TCA, Gálvez EJC, Smit N, Neuhaus K, Wang J, Baines JF, Abt B, Stecher B. 2019. Sequence and cultivation study of Muribaculaceae reveals novel species, host preference, and functional potential of this yet undescribed family. Microbiome. 7:1–15. doi:10.1186/s40168-019-0637-2.
  • Lebeda A, Luhová L, Sedlářová M, Jančová D. 2001. The role of enzymes in plant- fungal pathogens interactions. Journal of Plant Diseases and Protection. 89–111.
  • Letunic I, Bork P. 2021. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49:W293–W296. doi:10.1093/nar/gkab301.
  • Lin H, Peddada SD. 2020. Analysis of compositions of microbiomes with bias correction. Nat Commun. 11:3514. doi:10.1038/s41467-020-17041-7.
  • Liu Y, Ponpandian LN, Kim H, Jeon J, Hwang BS, Lee SK, Park S-C, Bae H. 2019. Distribution and diversity of bacterial endophytes from four Pinus species and their efficacy as biocontrol agents for devastating pine wood nematodes. Sci Rep. 9:12461. doi:10.1038/s41598-019-48739-4.
  • Lombard L, Crous PW. 2012. Phylogeny and taxonomy of the genusGliocladiopsis. Persoonia - Molecular Phylogeny and Evolution of Fungi. 28:25–33. doi:10.3767/003158512X635056.
  • Mahmood A, Turgay OC, Farooq M, Hayat R. 2016. Seed biopriming with plant growth promoting rhizobacteria: a review. FEMS Microbiol Ecol. 92:112. doi:10.1093/femsec/fiw112.
  • Malabrigo Jr P, Tobias AB, Witono J, Mursidawati S, Susatya A, Yunoh Siti-Munirah M, Wicaksono A, Raihandhany R, Edwards S, Thorogood CJ. 2023. Most of the world's largest flowers (genus Rafflesia) are now on the brink of extinction. Plants, People & Planet.
  • Miao Y, Zhang X, Zhang G, Feng Z, Pei J, Liu C, Huang L. 2023. From guest to host: parasite Cistanche deserticola shapes and dominates bacterial and fungal community structure and network complexity. Environmental Microbiome. 18:1–15. doi:10.1186/s40793-023-00471-3.
  • Molina J, Hazzouri KM, Nickrent D, Geisler M, Meyer RS, Pentony MM, Flowers JM, Pelser P, Barcelona J, Inovejas SA, et al. 2014. Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae). Mol Biol Evol. 31:793–803. doi:10.1093/molbev/msu051.
  • Molina J, McLaughlin W, Wallick K, Pedales R, Marius VM, Tandang DN, Damatac A, Stuhr N, Pell SK, Lim TM. 2017. Ex situ propagation of Philippine Rafflesia in the United States: challenges and prospects. Sibbaldia. 77–96.
  • Molina J, Nikolic D, Jeevarathanam JR, Abzalimov R, Park E-J, Pedales R, Mojica E-RE, Tandang D, McLaughlin W, Wallick K. 2022. Living with a giant, flowering parasite: metabolic differences between Tetrastigma loheri Gagnep. (Vitaceae) shoots uninfected and infected with Rafflesia (Rafflesiaceae) and potential applications for propagation. Planta. 255:1–12. doi:10.1007/s00425-021-03787-x.
  • Molina J, Sherpa C, Ng J, Sonam T, Stuhr N. 2018. Dna barcoding of online herbal supplements: crowd-sourcing pharmacovigilance in high school. Open Life Sciences. 13:48–55. doi:10.1515/biol-2018-0007.
  • Molina J, Wicaksono A, Michael TP, Kwak SH, Pedales RD, Joly-Lopez Z, Petrus S, Mamerto A, Tomek B, Ahmed S. 2023. The seed transcriptome of Rafflesia reveals horizontal gene transfer and convergent evolution: Implications for conserving the world's largest flower. Plants, People, Planet.
  • Msimbira LA, Smith DL. 2020. The roles of plant growth promoting microbes in enhancing plant tolerance to acidity and alkalinity stresses. Frontiers in Sustainable Food Systems. 4:106. doi:10.3389/fsufs.2020.00106.
  • Mursidawati S, Wicaksono A, da Silva JAT. 2019. Development of the endophytic parasite, Rafflesia patma Blume, among host plant (Tetrastigma leucostaphylum (Dennst.) Alston) vascular cambium tissue. S Afr J Bot. 123:382–386. doi:10.1016/j.sajb.2019.03.028.
  • Naqqash T, Imran A, Hameed S, Shahid M, Majeed A, Iqbal J, Hanif MK, Ejaz S, Malik KA. 2020. First report of diazotrophic Brevundimonas spp. as growth enhancer and root colonizer of potato. Sci Rep. 10:12893. doi:10.1038/s41598-020-69782-6.
  • Ng SM, Lee XW, Mat-Isa MN, Aizat-Juhari MA, Adam JH, Mohamed R, Wan KL, Firdaus-Raih M. 2018. Comparative analysis of nucleus-encoded plastid-targeting proteins in Rafflesia cantleyi against photosynthetic and non-photosynthetic representatives reveals orthologous systems with potentially divergent functions. Sci Rep. 8:17258. doi:10.1038/s41598-018-35173-1.
  • Nikolov LA, Tomlinson PB, Manickam S, Endress PK, Kramer EM, Davis CC. 2014. Holoparasitic Rafflesiaceae possess the most reduced endophytes and yet give rise to the world's largest flowers. Ann Bot. 114:233–242. doi:10.1093/aob/mcu114.
  • Oren A, Garrity GM. 2021. Valid publication of the names of forty-two phyla of prokaryotes. Int J Syst Evol Microbiol. 71:005056.
  • Pelser PB, Nickrent DL, Barcelona JF. 2016. Untangling a vine and its parasite: host specificity of PhilippineRafflesia(Rafflesiaceae). Taxon. 65:739–758. doi:10.12705/654.4.
  • Pelser PB, Nickrent DL, van Ee BW, Barcelona JF. 2019. A phylogenetic and biogeographic study of Rafflesia (Rafflesiaceae) in the Philippines: limited dispersal and high island endemism. Mol Phylogenet Evol. 139:106555. doi:10.1016/j.ympev.2019.106555.
  • Pereyra MM, Diaz MA, Meinhardt F, Dib JR. 2020. Effect of stress factors associated with postharvest citrus conditions on the viability and biocontrol activity of Clavispora lusitaniae strain 146. PLoS One. 15:e0239432. doi:10.1371/journal.pone.0239432.
  • Petrosyan K, Thijs S, Piwowarczyk R, Ruraż K, Vangronsveld J, Kaca W. 2022. Characterization and diversity of seed endophytic bacteria of the endemic holoparasitic plantCistanche armena(Orobanchaceae) from a semi-desert area in Armenia. Seed Sci Res. 32:264–273. doi:10.1017/S0960258522000204.
  • Poitevin CG, Veronesi RS, Pimentel IC, Auer CG. 2020. Foliar application of endophyticWickerhamomyces anomalusagainst grey mould inEucalyptus dunnii. Biocontrol Sci Technol. 30:93–102. doi:10.1080/09583157.2019.1687645.
  • Promputtha I, Lumyong S, Dhanasekaran V, McKenzie EHC, Hyde KD, Jeewon R. 2007. A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microb Ecol. 53:579–590. doi:10.1007/s00248-006-9117-x.
  • Rabosto X, Carrau M, Paz A, Boido E, Dellacassa E, Carrau FM. 2006. Grapes and vineyard soils as sources of microorganisms for biological control ofbotrytis cinerea. Am J Enol Vitic. 57:332–338. doi:10.5344/ajev.2006.57.3.332.
  • Raghav D, Jyoti A, Siddiqui AJ, Saxena J. 2022. Plant-associated endophytic fungi as potential bio-factories for extracellular enzymes: progress, challenges and strain improvement with precision approaches. J Appl Microbiol. 133:287–310. doi:10.1111/jam.15574.
  • Rajoka MI, Malik KA. 1999. Cellulomonas. In: R. K. Robinson, editor. Pages 365-371 in: encyclopedia of food microbiology. ed. San Diego, CA: Elsevier.
  • Refaei J, Jones EBG, Sakayaroj J, Santhanam J. 2011. Endophytic fungi from Rafflesia cantleyi: species diversity and antimicrobial activity. Mycosphere. 2:429–447.
  • Reis VM, Teixeira K. 2015. Nitrogen fixing bacteria in the familyAcetobacteraceaeand their role in agriculture. J Basic Microbiol. 55:931–949. doi:10.1002/jobm.201400898.
  • Rosenberg E, Zilber-Rosenberg I. 2018. The hologenome concept of evolution after 10 years. Microbiome. 6:1–14. doi:10.1186/s40168-018-0457-9.
  • Rowntree JK, Cameron DD, Preziosi RF. 2011. Genetic variation changes the interactions between the parasitic plant-ecosystem engineerRhinanthusand its hosts. Philos Trans R Soc, B. 366:1380–1388. doi:10.1098/rstb.2010.0320.
  • Ruraż K, Przemieniecki SW, Piwowarczyk R. 2023. Interspecies and temporal dynamics of bacterial and fungal microbiomes of pistil stigmas in flowers in holoparasitic plants of the Orobanche series Alsaticae (Orobanchaceae). Sci Rep. 13:6749. doi:10.1038/s41598-023-33676-0.
  • Sabra W, Quitmann H, Zeng A-P, Dai JY, Xiu Z-L. 2011. Microbial production of 2,3-butanediol. St. Louis, MO: Academic Press.
  • Sadeghi F, Samsampour D, Seyahooei MA, Bagheri A, Soltani J. 2019. Diversity and spatiotemporal distribution of fungal endophytes associated with citrus reticulata cv. siyahoo. Curr Microbiol. 76:279–289. doi:10.1007/s00284-019-01632-9.
  • Sahu, S., Prakash, A., and Shende, K. 2019. Talaromyces trachyspermus, an endophyte from Withania somnifera with plant growth promoting attributes. 2:13-21.
  • Sakamoto M, Ohkuma M. 2013. Bacteroides reticulotermitis sp. nov., isolated from the gut of a subterranean termite (Reticulitermes speratus). Int J Syst Evol Microbiol. 63:691–695. doi:10.1099/ijs.0.040931-0.
  • Sawana A, Adeolu M, Gupta RS. 2014. Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet. 5:429. doi:10.3389/fgene.2014.00429.
  • Sevilla M, De Oliveira A, Baldani IVO, Kennedyl C. 1998. Contributions of the bacterial endophyte Acetobacter diazotrophicus to sugarcane nutrition: a preliminary study. Symbiosis.
  • Shahzad R, Khan AL, Bilal S, Asaf S, Lee I-J. 2018. What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Front Plant Sci. 9:24. doi:10.3389/fpls.2018.00024.
  • Sharifi R, Ryu C-M. 2018. Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future. Ann Bot. 122:349–358. doi:10.1093/aob/mcy108.
  • Subhashini DV. 2015. Growth promotion and increased potassium uptake of tobacco by potassium-mobilizing bacteriumfrateuria aurantiagrown at different potassium levels in vertisols. Commun Soil Sci Plant Anal. 46:210–220. doi:10.1080/00103624.2014.967860.
  • Tapia-Hernández A, Bustillos-Cristales MR, Jiménez-Salgado T, Caballero-Mellado J, Fuentes-Ramirez LE. 2000. Natural endophytic occurrence of Acetobacter diazotrophicus in pineapple plants. Microb Ecol. 39:49–55. doi:10.1007/s002489900190.
  • Tedersoo L, Smith ME. 2013. Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev. 27:83–99. doi:10.1016/j.fbr.2013.09.001.
  • Thomas P, Sahu PK. 2021. Vertical transmission of diverse cultivation-recalcitrant endophytic bacteria elucidated using watermelon seed embryos. Front Microbiol. 12:635810. doi:10.3389/fmicb.2021.635810.
  • Tobias A, Thorogood CJ, Malabrigo P. 2023. The reinstatement of Rafflesia banaoana (Rafflesiaceae), and implications for assessing species diversity and conservation requirements of the world's largest flowers. Phytotaxa. 612:201–216. doi:10.11646/phytotaxa.612.2.5.
  • Toghueo RMK, Boyom FF. 2020. Endophytic Penicillium species and their agricultural, biotechnological, and pharmaceutical applications. 3 Biotech. 10:107.
  • Truyens S, Weyens N, Cuypers A, Vangronsveld J. 2015. Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep. 7:40–50. doi:10.1111/1758-2229.12181.
  • Uchiyama T, Uchihashi T, Nakamura A, Watanabe H, Kaneko S, Samejima M, Igarashi K. 2020. Convergent evolution of processivity in bacterial and fungal cellulases. Proc Natl Acad Sci USA. 117:19896–19903. doi:10.1073/pnas.2011366117.
  • Vandana UK, Rajkumari J, Singha LP, Satish L, Alavilli H, Sudheer PDVN, Chauhan S, Ratnala R, Satturu V, Mazumder PB. 2021. The endophytic microbiome as a hotspot of synergistic interactions, with prospects of plant growth promotion. Biology (Basel). 10:101. doi:10.3390/biology10020101.
  • Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A. 2015. The importance of the microbiome of the plant holobiont. New Phytol. 206:1196–1206. doi:10.1111/nph.13312.
  • Vujanovic V, Germida JJ. 2017. Seed endosymbiosis: a vital relationship in providing prenatal care to plants. Canadian Jorunal of Plant Science. 97:972–981.
  • Wee SL, Tan SB, Jürgens A. 2018. Pollinator specialization in the enigmatic Rafflesia cantleyi: A true carrion flower with species-specific and sex-biased blow fly pollinators. Phytochemistry. 153:120–128. doi:10.1016/j.phytochem.2018.06.005.
  • Wicaksono A, Mursidawati S, Molina J. 2021. A plant within a plant: insights on the development of the rafflesia endophyte within its host. The Botanical Review. 87:233–242. doi:10.1007/s12229-020-09236-w.
  • Wicaksono A, Mursidawati S, Sukamto LA, Teixeira da Silva JA. 2016. Rafflesia spp.: propagation and conservation. Planta. 244:289–296. doi:10.1007/s00425-016-2512-8.
  • Wu M-R, Chou T-S, Huang C-Y, Hsiao J-K. 2020. A potential probiotic- Lachnospiraceae NK4A136 group: Evidence from the restoration of the dietary pattern from a high-fat diet.
  • Xi Z, Bradley RK, Wurdack KJ, Wong K, Sugumaran M, Bomblies K, Rest JS, Davis CC. 2012. Horizontal transfer of expressed genes in a parasitic flowering plant. BMC Genomics. 13:227. doi:10.1186/1471-2164-13-227.
  • Xi Z, Wang Y, Bradley RK, Sugumaran M, Marx CJ, Rest JS, Davis CC. 2013. Massive mitochondrial gene transfer in a parasitic flowering plant clade. PLoS Genet. 9:e1003265. doi:10.1371/journal.pgen.1003265.
  • Xia Y, Sahib MR, Amna A, Opiyo SO, Zhao Z, Gao YG. 2019. Culturable endophytic fungal communities associated with plants in organic and conventional farming systems and their effects on plant growth. Sci Rep. 9:1669. doi:10.1038/s41598-018-38230-x.
  • Yang ZZ, Wafula EK, Honaas LA, Zhang HT, Das M, Fernandez-Aparicio M, Huang K, Bandaranayake PCG, Wu B, Der JP, et al. 2015. Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty. Mol. Biol. Evol. 32:767–790.
  • Yin C, Casa Vargas JM, Schlatter DC, Hagerty CH, Hulbert SH, Paulitz TC. 2021. Sensitive universal detection of blood parasites by selective pathogen-DNA enrichment and deep amplicon sequencing. Microbiome. 9:1–18. doi:10.1186/s40168-020-00939-1.
  • Zakaria L, Ning CH. 2013. Endophytic fusarium spp. from roots of lawn grass (Axonopus compressus). Trop Life Sci Res. 24:85.