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Effect of plant–soil feedbacks on the growth and competition of Lactuca species

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Abstract

Plant species generate specific soil communities that feedback on plant growth and competition. These feedbacks have been implicated in plant community composition and dispersion. We used Lactuca sativa and its wild progenitor Lactuca serriola to test the hypotheses that separate Lactuca species generate unique soil communities and that these soil communities differentially influence host, and neighboring, plant growth and competition. We grew each Lactuca in competition with the other, in sterile and non-sterile soils. We then examined the growth of each Lactuca species in sterile, non-sterile, and preconditioned soil. Finally, we used TRFLP techniques to explore whether the two Lactuca species generate significantly different bacterial communities in their rhizosphere soils. L. sativa proved to be the stronger competitor of the two species. However, sterilization increased the competitive effect of L. serriola background competitors. The growth experiment showed a significant effect on plant species, soil treatment, and the interaction of the two. Preconditioning soil caused reduced growth in both Lactuca species. Only L. serriola showed significantly increased growth in sterile soils. Our TRFLP analysis showed that the L. sativa soil community was significantly less diverse and that soil preconditioning had the largest impact on the community composition. These results show that Lactuca serriola’s rhizosphere communities generate a stronger negative feedback for plant growth than do the communities associated with L. sativa. Our study suggests that selection for plants that are able to grow in dense monoculture may have released Lactuca from species-specific negative soil feedbacks. This has important implications for both agriculture and the evolution of invasive plant species.

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References

  • Abbot KC, Karst J, Biederman LA, Borrett SR, Hastings A, Walsh V, Bever JD (2015) Spatial heterogeneity in soil microbes alters outcomes of plant competition. PLoS ONE. doi:10.1371/journal.pone.0125788

    PubMed  PubMed Central  Google Scholar 

  • Aguilera AG (2011) The influence of soil community density on plant-soil feedbacks: an important unknown in plant invasion. Ecol Model 222(18):3413–3420

    Article  Google Scholar 

  • Aguilera AG, Colon-Carmona A, Kesseli R, Dukes JS (2011) No accession-specific effect of rhizosphere communities on the growth and competition of arabidopsis thaliana accessions. PLoS ONE 6(11):1–8

    Article  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. Microb Ecol 68:1–13

    Article  CAS  Google Scholar 

  • Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157(3):465–473

    Article  Google Scholar 

  • Bever JD, Morton JB, Antonovics J, Schultz PA (1996) Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J Ecol 84(1):71–82

    Article  Google Scholar 

  • Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573

    Article  Google Scholar 

  • Bonanomi G, Giannino F, Mazzoleni S (2005) Negative plant-soil feedback and species coexistence. Oikos 111:311–321

    Article  Google Scholar 

  • Bremer C, Braker G, Matthies D, Reuter A, Engles C, Conrad R (2007) Impact of plant functional group, plant species, and sampling time on the competition of nirK-type denitrifier communities in soil. Appl Environ Microbiol 68:3067–3075

    Google Scholar 

  • Briones AM, Okabe S, Umemiya Y, Ramsing N, Reichardt W, Okuyama H (2002) Influence of different cultivars on populations of ammonia-oxidizing bacteria in the root environment of rice. Appl Environ Microbiol 74:738–744

    Google Scholar 

  • Bukowski AR, Peterman JS (2014) Intraspecific plant-soil feedback and intraspecific overyielding in Arabidopsis thaliana. Ecol Evol 4(12):2533–2545

    Article  PubMed  PubMed Central  Google Scholar 

  • Cardinale M, Grube M, Erlacher A et al (2015) Bacterial networks and co-occurrence relationships in the lettuce root microbiota. Environmental Microbiology 17(1):239–252

    Article  CAS  PubMed  Google Scholar 

  • Casper BB, Castelli JP (2007) Evaluating plant-soil feedbacks together with competition in a serpentine grassland. Ecol Lett 10:394–400

    Article  PubMed  Google Scholar 

  • Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinform 10:171

    Article  Google Scholar 

  • de Vries IM (1990) Crossing experiments of lettuce cultivars and species (lactuca sect, lactuca, compositae). Plant Syst Evol 171(1–4):233–248

    Article  Google Scholar 

  • Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6(6):503–523

    Article  CAS  Google Scholar 

  • Fox J, Weisberg S, Bates D (2010) car: Companion to Applied Regression. R package version 2.0-2

  • Goldberg DE, Barton AM (1992) Patterns and consequences of interspecific competition in natural communities: a review of field experiments with plants. Am Nat 139(4):771–801

    Article  Google Scholar 

  • Grayston SJ, Prescott CE (2005) Microbial communities in forest floors under four tree species in coastal British Columbia. Soil Biol Biochem 37(6):1157–1167

    Article  CAS  Google Scholar 

  • Haney CH, Samuel BS, Bush J, Ausubel F (2015) Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nat Plants. doi:10.1038/nplants.2015.51

    PubMed  PubMed Central  Google Scholar 

  • Heinze J, Werner T, Weber E, Rillig MC, Joshi J (2015) Soil biota effects on local abundances of three grass species along a land-use gradient. Oecologia 179(1):249–259

    Article  CAS  PubMed  Google Scholar 

  • Hendriks M, Ravenek JM, Smit-Tiekstra AE, van der Paauw JW, de Caluwe H, van der Putten WH, de Kroon H, Mommer L (2015) Spatial heterogeneity of plant-soil feedback affects root interactions and interspecific competition. New Phyt. 207:830–840

    Article  Google Scholar 

  • Hill M, Witsenboer H, Zabeau M, Vos P, Kesseli R, Michelmore R (1996) Amplified fragment length polymorphisms (AFLPs) as a tool for assessing the genetic relationships in Lactuca spp. Theor Appl Genet 93:1202–1210

    Article  CAS  PubMed  Google Scholar 

  • Jost L (2006) Entropy and diversity. Oikos 113:363–375

    Article  Google Scholar 

  • Kardol P, Bezemer TM, van der Putten WH (2006) Temporal variation in plant-soil feedback controls succession. Ecol Lett 9:1080–1088

    Article  PubMed  Google Scholar 

  • Kardol P, Cornips NJ, van Kempen MML, Bakx-Schotman JMT, van der Putten WH (2007) Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol Monographs 77(2):147–162

    Article  Google Scholar 

  • Kesseli R, Michelmore R (1996) The compositae: systematically fascinating but specifically neglected. In: Paterson A (ed) Genome mapping in plants. Landes Press, Georgetown, pp 181–194

    Google Scholar 

  • Kesseli R, Ochoa O, Michelmore R (1991) Variation at RFLP loci in Lactuca spp. and origin of cultivated lettuce (L. sativa). Genome 34(3):430–436

    Article  Google Scholar 

  • Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70

    Article  CAS  PubMed  Google Scholar 

  • Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11(9):980–992

    Article  PubMed  Google Scholar 

  • Kulmatiski A, Beard KH, Grenzer J, Forero L, Heavilin J (2016) Using plant-soil feedbacks to predict plant biomass in diverse communities. Ecology 97(8):2064–2073

    Article  PubMed  Google Scholar 

  • Lebeda A, Dolezalova I, Kristkova E, Mieslerova B (2001) Biodiversity and ecogeography of wild Lactuca spp. in some European countries. Genet Resour Crop Evol 48:153–164

    Article  Google Scholar 

  • Levin JM, Adler PB, Yelenick SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989

    Article  Google Scholar 

  • Lindqvist K (1960) Cytogenetic studies in the serriola group of Lactuca. Hereditas. 46(1–2):75–151

    Google Scholar 

  • Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755

    Article  CAS  PubMed  Google Scholar 

  • Maron JL, Smith AL, Ortega YK, Pearson DE, Callaway RM (2016) Negative plant-soil feedbacks increase with plant abundance, and are unchanged by competition. Ecology 97(8):2055–2063

    Article  PubMed  Google Scholar 

  • Masclaux F, Hammond RL, Meunier J, Gouhier-Darimont C, Keller L, Reymond P (2010) Competitive ability not kinship affects growth of arabidopsis thaliana accessions. New Phytol 185(1):322–331

    Article  CAS  PubMed  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • Micallef SA, Shiaris MP, Colon-Carmona A (2009) Influence of arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60(6):1729–1742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris WF, Hufbauer RA, Agrawal AA, Bever JD, Borowicz VA, Gilber GS et al (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029

    Article  PubMed  Google Scholar 

  • Nocker A, Burr M, Camper AK (2007) Genotypic microbial community profiling: a critical technical review. Microb Ecol 54:276–289

    Article  CAS  PubMed  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community ecology package 10

  • Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J (2015) Selection on soil microbes reveals reproducible impacts on plant function. ISME J 9:980–989

    Article  CAS  PubMed  Google Scholar 

  • Parepa M, Fischer M, Bossdorf O (2013) Environmental variability promotes plant invasion. Commun. doi:10.1038/ncomms2632

    Google Scholar 

  • Pendergast TH IV, Burke DJ, Carson WP (2013) Belowground biotic community drives aboveground dynamics: a test of the soil community feedback model. New Phytol 197:1300–1310

    Article  PubMed  Google Scholar 

  • Polz M, Cavanaugh C (1998) Bias in product-to-template ratios in multitemplate PCR. Appl Environ Microbiol 64:3724–3730

    CAS  PubMed  PubMed Central  Google Scholar 

  • Priha O, Grayston SJ, Hiukka R, Pennanen T, Smolander A (2001) Microbial community structure and characteristics of the organic matter in soils under pinus sylvestris, picea abies and betula pendula at two forest sites. Biol Fertil Soils 33(1):17–24

    Article  CAS  Google Scholar 

  • Raaijamkers JM, Paulitz CT, Steinberg C, Alabouvette C, Moennne-Loccoz T (2009) The rhizosphere: a playground for soilborne pathogens and beneficial microorganisms. Plant Soil. doi:10.1007/s11104-008-9568-6

    Google Scholar 

  • Ralser M, Querfurth R, Warnatz H-J, Lehrach H, Yaspo M-L, Krobitsch S (2006) An efficient and economic enhancer mix for PCR. Biochem Biophys Res Commun 347:747–751

    Article  CAS  PubMed  Google Scholar 

  • Reinhart KO (2012) The organization of plant communities: negative plant-soil feedbacks and semiarid grasslands. Ecology 93(11):2377–2385

    Article  PubMed  Google Scholar 

  • Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170(3):445–457

    Article  PubMed  Google Scholar 

  • Reinhart KO, Packer A, Van der Putten WH, Clay K (2003) Plant-soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol Lett 6:1046–1050

    Article  Google Scholar 

  • Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562

    Article  Google Scholar 

  • Ryder EJ, Whitaker TW, Lettuce NE, Simmonds (eds) (1976) Evolution of crop plants. Longman Group Ltd., London

  • Schlaeppi K, Dombrowski N, Oter RG, van Themaat EVL, Schulze-Lefert P (2014) Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc Natl Acad Sci 111:585–592

  • Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV, Whitham TG, Hart SC (2008) Plant-soil- microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89(3):773–781

    Article  PubMed  Google Scholar 

  • Stoffel K, van Leeuwen H, Kozik A, Caldwell D, Ashrafi H, Cui X, Tan X, Hill T, Reyes-Chin-Wo S, Truco M-J (2012) Development and application of a 6.5 million feature Affymetrix Genechip® for massively parallel discovery of single position polymorphisms in lettuce (Lactuca spp.). BMC Genom 13:1

    Article  Google Scholar 

  • Templer P, Findlay S, Lovett G (2003) Soil microbial biomass and nitrogen transformations among five tree species of the Catskill Mountains, New York. USA. Soil Biol Biochem. 35(4):607–613

    Article  CAS  Google Scholar 

  • terHorst CP, Zee PC (2016) Eco-evolutionary dynamics in plant-soil feedbacks. Funct Ecol 30:1062–1072

    Article  Google Scholar 

  • Trevors JT (1996) Sterilization and inhibition of microbial activity in soil. J Microbiol Methods 26:53–59

    Article  CAS  Google Scholar 

  • Truco MJ, Antonise R, Lavelle D, Ochoa O, Kozik A, Witsenboer H, Fort S, Jeuken M, Kesseli R, Lindhout P, Michelmore R, Peleman J (2007) A high-density integrated genetic linkage map of lettuce (Lactuca spp.). Theor Appl Genet 115:735–746

    Article  CAS  PubMed  Google Scholar 

  • Uwimana B, Smulders MJ, Hooftman DA, Hartman Y, van Tienderen PH, Jansen J, McHale LK, Michelmore RW, van de Wiel CC, Visser RG (2012) Hybridization between crops and wild relatives: the contribution of cultivated lettuce to the vigour of crop-wild hybrids under drought, salinity and nutrient deficiency conditions. Theor Appl Genet 125(6):1097–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Nuland ME, Wooliver RC, Pfennigwerth AA, Read QD, Ware IM, Mueller L, Fordyce JA, Schweitzer JA, Bailey JK (2016) Plant-soil feedback: connecting ecosystem ecology and evolution. Funct Ecol 30:1032–1042

    Article  Google Scholar 

  • Wagner MR, Lundberg DS, Coleman-Derr D, Tringe SG, Dangl JL, Mitchell-Olds T (2014) Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecol Lett 17:717–726

    Article  PubMed  PubMed Central  Google Scholar 

  • Westover KM, Bever JD (2001) Mechanisms of plant species coexistence: roles of rhizosphere bacteria and root fungal pathogens. Ecology 82(12):3285–3294

    Article  Google Scholar 

  • Wickham H (2011) The split-apply-combine strategy for data analysis. J Stat Softw 40:1–29

    Google Scholar 

  • Wilson SD, Tilman D (1991) Components of plant competition along an experimental gradient of nitrogen availability. Ecology 72:1050–1065

  • Xiong S, Nilsson CJ (1999) The effects of plant litter on vegetation: a meta-analysis. Ecology 87:984–994

    Article  Google Scholar 

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Acknowledgements

This work was funded in part by the National Science Foundation grants IOS 0847691 and DBI 0820451, and The University of Massachusetts, Boston. We also thank anonymous reviewers for their helpful comments and suggestions.

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Authors and Affiliations

  1. Biology Department, Simmons College, 300 The Fenway, Boston, MA, 02115, USA

    Anna G. Aguilera

  2. Biology Department, University of Massachusetts, Boston, 100 Morrissey Boulevard, Boston, MA, 02125, USA

    Stuart Morey, Melinda Gammon, Monica Jiang, Saimom Ramos & Rick Kesseli

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  1. Anna G. Aguilera
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  2. Stuart Morey
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  3. Melinda Gammon
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  4. Monica Jiang
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Correspondence to Anna G. Aguilera.

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Communicated by Lori Biederman.

Appendix

Appendix

See Fig. 6.

Fig. 6
figure 6

Schematic diagram of the Competition experiment’s experimental design. Each circle represents an experimental treatment. SAT a single Lactuca sativa plant. SER a single Lactuca serriola plant. This design was replicated in sterilized and non-sterilized soil

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Aguilera, A.G., Morey, S., Gammon, M. et al. Effect of plant–soil feedbacks on the growth and competition of Lactuca species. Plant Ecol 218, 359–372 (2017). https://doi.org/10.1007/s11258-016-0697-3

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