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Successional adaptive strategies revealed by correlating arbuscular mycorrhizal fungal abundance with host plant gene expression
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  • Cheng Gao,
  • Pierre-Emmanuel Courty,
  • Nelle Varoquaux,
  • Benjamin Cole,
  • Liliam Montoya,
  • Ling Xu,
  • Elizabeth Purdom,
  • John Vogel,
  • Robert Hutmacher,
  • Jeffery Dahlberg,
  • Devin Colemann-Derr,
  • Peggy Lemaux,
  • John Taylor
Cheng Gao
University of California Berkeley

Corresponding Author:gaoc@im.ac.cn

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Pierre-Emmanuel Courty
Agroécologie, AgroSup Dijon, CNRS, Université de Bourgogne, INRAE, Université de Bourgogne Franche-Comté, Dijon, France.
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Nelle Varoquaux
University of California Berkeley
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Benjamin Cole
US Department of Energy Joint Genome Institute
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Liliam Montoya
University of California Berkeley
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Ling Xu
University of California Berkeley
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Elizabeth Purdom
University of California Berkeley
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John Vogel
US Department of Energy Joint Genome Institute
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Robert Hutmacher
University of California West Side Research and Extension Center
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Jeffery Dahlberg
University of California Kearney Agricultural Research and Extension Center
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Devin Colemann-Derr
University of California Berkeley
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Peggy Lemaux
University of California Berkeley
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John Taylor
University of California Berkeley
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Abstract

Arbuscular mycorrhizal fungi (AMF), the mutualistic symbionts with most crops, constitute a research system of human-associated fungi whose relative simplicity and synchrony are conducive to experimental ecology. However, little is known about the shifts in adaptive strategies of sorghum associated AMFs where strong AMF succession replaces initially ruderal species with competitive ones and where the strongest plant response to drought is to manage these AMF. First, we hypothesize that, when irrigation is stopped to mimic drought, competitive AMF species should be replaced by AMF species tolerant to drought stress. We then, for the first time, correlate AMF abundance and host plant transcription to test two novel hypotheses about the mechanisms behind the shift from ruderal to competitive AMF. Surprisingly, despite imposing drought stress, we found no stress tolerant AMF. Remarkably, we found strong and differential correlation between the successional shift from ruderal to competitive AMF and sorghum genes whose products (i) produce and release strigolactone signals, (ii) perceive mycorrhizal-lipochitinoligosaccharide (Myc-LCO) signals, (iii) provide plant lipid and sugar to AMF and, (iv) import minerals and water provided by AMF. These novel insights into host gene expression and succession of AMF show adaptive strategies evolved by AMF and their hosts and provide a rationale for selecting AMF to reduce inputs and maximize yield in commercial agriculture. Future research opportunities include testing the specifics and generality of our hypotheses by employing genetically modified host plants, and exploring additional genes underlying the adaptive strategies in natural succession.
18 May 2021Submitted to Molecular Ecology
25 May 2021Submission Checks Completed
25 May 2021Assigned to Editor
23 Jun 2021Reviewer(s) Assigned
21 Jul 2021Review(s) Completed, Editorial Evaluation Pending
24 Aug 2021Editorial Decision: Revise Minor
18 Sep 2021Review(s) Completed, Editorial Evaluation Pending
18 Sep 20211st Revision Received
19 Sep 2021Reviewer(s) Assigned
09 Nov 2021Editorial Decision: Revise Minor
02 Dec 2021Review(s) Completed, Editorial Evaluation Pending
02 Dec 20212nd Revision Received
23 Dec 2021Editorial Decision: Accept
09 Jan 2022Published in Molecular Ecology. 10.1111/mec.16343