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Aromatic amino acid biosynthesis impacts root hair development and symbiotic associations in Lotus japonicus

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posted on 2023-11-21, 05:25 authored by Jesus Montiel, Ivette Garcia-Soto, Euan K James, Dugald ReidDugald Reid, Luis Cardenas, Selene Napsucialy-Mendivil, Shaun Ferguson, Joseph G Dubrovsky, Jens Stougaard
Legume roots can be symbiotically colonized by arbuscular mycorrhizal (AM) fungi and nitrogen-fixing bacteria. In Lotus japonicus, the latter occurs intracellularly by the cognate rhizobial partner Mesorhizobium loti or intercellularly with the Agrobacterium pusense strain IRBG74. Although these symbiotic programs show distinctive cellular and transcriptome signatures, some molecular components are shared. In this study, we demonstrate that 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase 1 (DAHPS1), the first enzyme in the biosynthetic pathway of aromatic amino acids (AAAs), plays a critical role in root hair development and for AM and rhizobial symbioses in Lotus. Two homozygous DAHPS1 mutants (dahps1-1 and dahps1-2) showed drastic alterations in root hair morphology, associated with alterations in cell wall dynamics and a progressive disruption of the actin cytoskeleton. The altered root hair structure was prevented by pharmacological and genetic complementation. dahps1-1 and dahps1-2 showed significant reductions in rhizobial infection (intracellular and intercellular) and nodule organogenesis and a delay in AM colonization. RNAseq analysis of dahps1-2 roots suggested that these phenotypes are associated with downregulation of several cell wall-related genes, and with an attenuated signaling response. Interestingly, the dahps1 mutants showed no detectable pleiotropic effects, suggesting a more selective recruitment of this gene in certain biological processes. This work provides robust evidence linking AAA metabolism to root hair development and successful symbiotic associations.

Funding

This work was supported by the Bill & Melinda Gates Foundation (OPP11772165; grant Engineering the Nitrogen Symbiosis for Africa made to the University of Cambridge), the H2020 European Research Council, research and innovation programme (grant agreement no. 834221), the Consejo Nacional de Ciencia y Tecnología (CONACyT, grant A1-S-9236), and Dirección General de Asuntos del Personal Académico—Universidad Nacional Autónoma de México (UNAM)—Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT, grant IA200723 and IN204221). I.G.-S. was granted with a PhD scholarship of CONACyT (856458).

History

Publication Date

2023-10-01

Journal

Plant Physiology

Volume

193

Issue

2

Pagination

19p. (p. 1508-1526)

Publisher

American Society of Plant Biologists

ISSN

0032-0889

Rights Statement

© The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

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