Polyploidy and plant-fungus symbiosis: evidence of cytotype-specific microbiomes in the halophyte Salicornia (Amaranthaceae)

Polyploidy is recognized as a mechanism of speciation in plants with cascading effects on biotic interactions. However, a limited number of studies have investigated the effects of polyploidy on the association of plants and microorganisms. Herein, we investigated whether two Salicornia cytotypes (S. europaea – 2x and S. procumbens – 4x) show different root-associated fungal communities. Additionally, we explored the existence of cytotype-specific root anatomical traits, which could influence fungal recruitment and establishment. Salicornia spp. were identified based on their ploidy level. The root-associated fungal microbiome of Salicornia was analyzed using high throughput amplicon sequencing (ITS1 of rDNA) in spring and summer. The following root anatomical traits were investigated: maximum root diameter, periderma thickness, parenchyma thickness, diameter of the vascular cylinder and maximum diameter of parenchyma cells. Our results showed that Shannon diversity and evenness indices were higher in samples of Salicornia procumbens (4x) compared to those of S. europaea (2x), and in summer the root-associated fungal community of S. procumbens (4x) was significantly different from that of S. europaea (2x). The orders Xylariales, Malasseziales and Pleosporales were the most frequent root colonizers in both cytotypes and most of the taxa associated with Salicornia were functionally classified as saprophytes or plant pathogens. Finally, we observed larger periderma and parenchyma layers in S. procumbens (4x) than S. europaea (2x) that may contribute to the observed differences in community composition between the two cytotypes. Our results suggest that differences in ploidy may modulate plant interaction with fungi by affecting species recruitment and microbiome structure. In addition, cytotype-specific root traits may also have the potential to affect differently community assembly in the two cytotypes.

[1]  D. Albach,et al.  Effects of fungal inoculation on the growth of Salicornia (Amaranthaceae) under different salinity conditions , 2021, Symbiosis.

[2]  D. Coleman-Derr,et al.  Evaluating domestication and ploidy effects on the assembly of the wheat bacterial microbiome , 2021, PloS one.

[3]  Irina S Druzhinina,et al.  Insight into a highly polymorphic endophyte isolated from the roots of the halophytic seepweed Suaeda salsa: Laburnicola rhizohalophila sp. nov. (Didymosphaeriaceae, Pleosporales). , 2020, Fungal biology.

[4]  J. Maul,et al.  Dark septate endophyte improves salt tolerance of native and invasive lineages of Phragmites australis , 2020, The ISME Journal.

[5]  T. Ashman,et al.  Polyploid plants obtain greater fitness benefits from a nutrient acquisition mutualism. , 2020, The New phytologist.

[6]  J. Maciá‐Vicente,et al.  Community sequencing on a natural experiment reveals little influence of host species and timing but a strong influence of compartment on the composition of root endophytes in three annual Brassicaceae , 2020, bioRxiv.

[7]  L. Hansen,et al.  Seasonal epiphytic microbial dynamics on grapevine leaves under biocontrol and copper fungicide treatments , 2020, Scientific Reports.

[8]  T. Ashman,et al.  Autopolyploidy alters nodule-level interactions in the legume-rhizobium mutualism. , 2019, American journal of botany.

[9]  J. Lynch,et al.  Root cortical anatomy is associated with differential pathogenic and symbiotic fungal colonization in maize. , 2019, Plant, cell & environment.

[10]  B. Furtado,et al.  A window into fungal endophytism in Salicornia europaea: deciphering fungal characteristics as plant growth promoting agents , 2019, Plant and Soil.

[11]  K. A. Segraves,et al.  Intraspecific polyploidy correlates with colonization by arbuscular mycorrhizal fungi in Heuchera cylindrica. , 2019, American journal of botany.

[12]  S. Urquiaga,et al.  Dark septate endophytic fungi increase the activity of proton pumps, efficiency of 15N recovery from ammonium sulphate, N content, and micronutrient levels in rice plants , 2019, Brazilian Journal of Microbiology.

[13]  M. Gołębiewski,et al.  Bacterial and Fungal Endophytic Microbiomes of Salicornia europaea , 2019, Applied and Environmental Microbiology.

[14]  J. Doyle,et al.  Polyploidy, the Nucleotype, and Novelty: The Impact of Genome Doubling on the Biology of the Cell , 2019, International Journal of Plant Sciences.

[15]  M. Gonçalves Three new species of Neocamarosporium isolated from saline environments: N. aestuarinum sp. nov., N. endophyticum sp. nov. and N. halimiones sp. nov. , 2019, Mycosphere.

[16]  J. Suda,et al.  Sympatric diploid and tetraploid cytotypes of Centaurea stoebe s.l. do not differ in arbuscular mycorrhizal communities and mycorrhizal growth response. , 2018, American journal of botany.

[17]  W. Boerjan,et al.  Polyploidy Affects Plant Growth and Alters Cell Wall Composition1[OPEN] , 2018, Plant Physiology.

[18]  Kyle C. Weber,et al.  ITSxpress: Software to rapidly trim internally transcribed spacer sequences with quality scores for marker gene analysis , 2018, F1000Research.

[19]  C. Dai,et al.  Mutualistic fungus Phomopsis liquidambari increases root aerenchyma formation through auxin-mediated ethylene accumulation in rice (Oryza sativa L.). , 2018, Plant physiology and biochemistry : PPB.

[20]  C. Schadt,et al.  Modification of plant cell wall chemistry impacts metabolome and microbiome composition in Populus PdKOR1 RNAi plants , 2018, Plant and Soil.

[21]  Eoin L. Brodie,et al.  Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly , 2018, Nature Microbiology.

[22]  T. Ashman,et al.  The direct effects of plant polyploidy on the legume–rhizobia mutualism , 2018, Annals of botany.

[23]  Brian Bushnell,et al.  BBMerge – Accurate paired shotgun read merging via overlap , 2017, PloS one.

[24]  Paul J. McMurdie,et al.  Exact sequence variants should replace operational taxonomic units in marker-gene data analysis , 2017, The ISME Journal.

[25]  B. Ewers,et al.  Polyploidy and the relationship between leaf structure and function: implications for correlated evolution of anatomy, morphology, and physiology in Brassica , 2017, BMC Plant Biology.

[26]  J. Maciá‐Vicente,et al.  Low diversity and abundance of root endophytes prevail throughout the life cycle of an annual halophyte , 2016, Mycological Progress.

[27]  L. A. Prather,et al.  The role of polyploidy in shaping morphological diversity in natural populations of Phlox amabilis. , 2016, American journal of botany.

[28]  Alga Zuccaro,et al.  Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. , 2016, Current opinion in microbiology.

[29]  K. A. Segraves,et al.  Species interactions and plant polyploidy. , 2016, American journal of botany.

[30]  Scott T. Bates,et al.  FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild , 2016 .

[31]  R. Nichols,et al.  Genome size and ploidy influence angiosperm species' biomass under nitrogen and phosphorus limitation , 2016, The New phytologist.

[32]  Heidi M. Meudt,et al.  Is genome downsizing associated with diversification in polyploid lineages of Veronica , 2015 .

[33]  Michael S. Barker,et al.  The butterfly plant arms-race escalated by gene and genome duplications , 2014, Proceedings of the National Academy of Sciences.

[34]  J. Suda,et al.  Intraspecific ploidy variation: A hidden, minor player in plant-soil-mycorrhizal fungi interactions. , 2014, American journal of botany.

[35]  Rob Knight,et al.  EMPeror: a tool for visualizing high-throughput microbial community data , 2013, GigaScience.

[36]  Satoshi Yamamoto,et al.  High-Coverage ITS Primers for the DNA-Based Identification of Ascomycetes and Basidiomycetes in Environmental Samples , 2012, PloS one.

[37]  H. Müller-Schärer,et al.  Influence of plant phenostage and ploidy level on oviposition and feeding of two specialist herbivores of spotted knapweed, Centaurea stoebe , 2012 .

[38]  J. Kadereit,et al.  Tetraploid European Salicornia species are best interpreted as ecotypes of multiple origin , 2011 .

[39]  J. Suda,et al.  Ploidy-specific interactions of three host plants with arbuscular mycorrhizal fungi: Does genome copy number matter? , 2010, American journal of botany.

[40]  M. Wildermuth Modulation of host nuclear ploidy: a common plant biotroph mechanism. , 2010, Current opinion in plant biology.

[41]  Pedro M. Valero-Mora,et al.  ggplot2: Elegant Graphics for Data Analysis , 2010 .

[42]  T. Vancov,et al.  Amplification of soil fungal community DNA using the ITS86F and ITS4 primers. , 2009, FEMS microbiology letters.

[43]  J. Lynch,et al.  Plant phenology: a critical controller of soil resource acquisition. , 2009, Journal of experimental botany.

[44]  S. Micallef,et al.  Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates , 2009, Plant signaling & behavior.

[45]  R. Sikora,et al.  Biological control of Radopholus similis in banana by combined application of the mutualistic endophyte Fusarium oxysporum strain 162, the egg pathogen Paecilomyces lilacinus strain 251 and the antagonistic bacteria Bacillus firmus , 2009, BioControl.

[46]  R. Kao Implications of Polyploidy in the Host Plant of a Dipteran Seed Parasite , 2008 .

[47]  D. Sokoloff,et al.  A taxonomic nightmare comes true: phylogeny and biogeography of glassworts (Salicornia L., Chenopodiaceae) , 2007 .

[48]  D. Haydon,et al.  Pollinator-mediated assortative mating in mixed ploidy populations of Chamerion angustifolium (Onagraceae) , 2006, Oecologia.

[49]  C. Pieterse,et al.  Significance of inducible defense-related proteins in infected plants. , 2006, Annual review of phytopathology.

[50]  J. Greilhuber,et al.  Flow cytometric and Feulgen densitometric analysis of genome size variation in Pisum , 1996, Theoretical and Applied Genetics.

[51]  James D. Bever,et al.  GRASSROOTS ECOLOGY: PLANT-MICROBE-SOIL INTERACTIONS AS DRIVERS OF PLANT COMMUNITY STRUCTURE AND DYNAMICS , 2003 .

[52]  P. Weathers,et al.  Tetraploid Artemisia annua hairy roots produce more artemisinin than diploids , 2003, Plant Cell Reports.

[53]  D. Dunigan,et al.  Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? , 2001, The New phytologist.

[54]  D. Schemske,et al.  Ecological mechanisms of reproductive isolation between diploid and tetraploid Chamerion angustifolium , 2000 .