Synergistic effects of canopy chemistry and autogenic soil biota on a global invader

  • Sudipto Majumdar
  • , Harleen Kaur
  • , Matthew J. Rinella
  • , Anish Kundu
  • , Jyothilakshmi Vadassery
  • , Nadir Erbilgin
  • , Ragan M. Callaway
  • , Marc W. Cadotte
  • , Inderjit

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

Soil biota have strong effects on plants, but we have a poor understanding of how plant chemistry might modify these effects. We examined the effect of soil biota associated with an exotic invasive tree, Prosopis juliflora, versus that associated with native species, from seven sites across India on conspecifics and two other plant species. We then measured changes in species-specific soil biota effects (identified as plant–soil feedbacks, PSFs) when leaf leachate from P. juliflora or from native plant species was added to soil containing respective live and sterile soil inoculum. We quantified the amino acid L-tryptophan from leaf leachate of P. juliflora, Leucaena leucocephala (another invader), and two native species. We also tested effects of P. juliflora or native species soil inoculum amendment of tryptophan on P. juliflora, P. cineraria and L. leucocephala across seven sites. We then quantified the microbially metabolized derivatives of tryptophan, phytohormone indole-3-acetic acid (IAA) and intermediates after adding tryptophan into P. juliflora and native soils. Soil biota associated with P. juliflora generated positive effects on conspecifics and L. leucocephala, but negative effects on the native congener P. cineraria. When P. juliflora leaf leachate was added to soil with live P. juliflora inoculum, PSFs became more positive for P. juliflora and other species, compared to leaf leachate amended with sterile soil inoculum. Native leaf leachate interacted weakly with soil biota to impact biomass of conspecifics and heterospecifics. There was roughly 10× more tryptophan in the leaf leachate of P. juliflora than in the leaf leachate of other species. Tryptophan generally increased positive PSFs associated with P. juliflora relative to soil biota associated with other plant species. When tryptophan was added to live P. juliflora soil, IAA and its intermediates were produced at five of seven sites, and at four of these sites soil biota from P. juliflora had positive PSFs. Synthesis. These results provide the first experimental evidence that a chemical leached from the leaves of an invader regulates PSFs. Our results indicate that canopy effects and PSFs, which are usually studied independently, can interact in ways that strongly affect conspecifics and neighbouring species.

Original languageEnglish
Pages (from-to)1497-1513
Number of pages17
JournalJournal of Ecology
Volume111
Issue number7
DOIs
StatePublished - Jul 2023

Funding

We thank Tarlok Chand, Vinod Maina, S.K. Thakur, Paramjit Singh, C.R. Babu, Guncha Ishangullyeva, Faiyaz A. Khudsar and Megha Ojha for their help in the field and/or during the conduct of experiments. Inderjit acknowledges financial assistance provided by the Department of Biotechnology, India (BT/PR6928/BCE/8/927/2012). RMC thanks the National Science Foundation EPSCoR Cooperative Agreement OIA‐1757351 for support. NE thanks the Natural Sciences and Engineering Research Council of Canada (Discovery Grant Program) for support and JV thanks Department of Biotechnology, India (BT/ INF/22/SP28268/2018) and NIPGR core grant for funding. The authors declare no competing interests. Inderjit conceived the research idea and funded the project; Sudipto Majumdar, Harleen Kaur and Inderjit designed the experiments; Sudipto Majumdar collected data on soil microbial effects (Experiments 1, 2 and 4) and prepared samples for RP‐UHPLC study; Anish Kundu, Sudipto Majumdar, Harleen Kaur and Jyothilakshmi Vadassery performed and analysed RP‐UHPLC data; Matthew J. Rinella developed the models and carried out statistical analyses; Harleen Kaur (Figures 1–6 ; Figures S3 , S6 and S7 ), Inderjit (Figures S1 , S4 , S6 and S7 ), and SM (Figure S8 ) prepared figures; Harleen Kaur, Ragan M. Callaway, Marc W. Cadotte, Nadir Erbilgin, Sudipto Majumdar and Inderjit interpreted the data. Inderjit wrote the first draft of the manuscript that was further developed by Ragan M. Callaway, Inderjit and Harleen Kaur, and then finalized by all authors. Nadir Erbilgin and Jyothilakshmi Vadassery funded RP‐UHPLC research at University of Alberta, Canada, and National Institute of Plant Genome Research, India respectively.

FundersFunder number
National Institute for Plant Genome Research
OIA‐1757351
BT/ INF/22/SP28268/2018
University of Alberta
BT/PR6928/BCE/8/927/2012

    Keywords

    • L-tryptophan
    • exotic species
    • indole 3-acetic acid
    • invasion
    • invasional meltdown
    • leaf leachate
    • plant–soil feedbacks
    • soil biota

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