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

Jesús Montiel; Ivette García-Soto; Euan K. James; Dugald Reid; Luis Cárdenas; Selene Napsucialy-Mendivil; Shaun Ferguson; Joseph G. Dubrovsky; Jens Stougaard

doi:10.1093/plphys/kiad398

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

Jesús Montiel^*, Ivette García-Soto, Euan K. James, Dugald Reid, Luis Cárdenas, Selene Napsucialy-Mendivil, Shaun Ferguson, Joseph G. Dubrovsky, Jens Stougaard^*

^*Corresponding author for this work

Department of Molecular Biology and Genetics - Plant Molecular Biology

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

5 Citations (Scopus)

Abstract

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.

Original language	English
Journal	Plant Physiology
Volume	193
Issue	2
Pages (from-to)	1508-1526
Number of pages	19
ISSN	0032-0889
DOIs	https://doi.org/10.1093/plphys/kiad398
Publication status	Published - Oct 2023

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@article{8ba927c630914bfa817bc0ff9e82dddb,

title = "Aromatic amino acid biosynthesis impacts root hair development and symbiotic associations in Lotus japonicus",

abstract = "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.",

author = "Jes{\'u}s Montiel and Ivette Garc{\'i}a-Soto and James, {Euan K.} and Dugald Reid and Luis C{\'a}rdenas and Selene Napsucialy-Mendivil and Shaun Ferguson and Dubrovsky, {Joseph G.} and Jens Stougaard",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.",

year = "2023",

month = oct,

doi = "10.1093/plphys/kiad398",

language = "English",

volume = "193",

pages = "1508--1526",

journal = "Plant Physiology",

issn = "0032-0889",

publisher = "American Society of Plant Biologists",

number = "2",

}

Aromatic amino acid biosynthesis impacts root hair development and symbiotic associations in Lotus japonicus. / Montiel, Jesús; García-Soto, Ivette; James, Euan K. et al.
In: Plant Physiology, Vol. 193, No. 2, 10.2023, p. 1508-1526.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Aromatic amino acid biosynthesis impacts root hair development and symbiotic associations in Lotus japonicus

AU - Montiel, Jesús

AU - García-Soto, Ivette

AU - James, Euan K.

AU - Reid, Dugald

AU - Cárdenas, Luis

AU - Napsucialy-Mendivil, Selene

AU - Ferguson, Shaun

AU - Dubrovsky, Joseph G.

AU - Stougaard, Jens

PY - 2023/10

Y1 - 2023/10

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85172425561&partnerID=8YFLogxK

U2 - 10.1093/plphys/kiad398

DO - 10.1093/plphys/kiad398

M3 - Journal article

C2 - 37427869

AN - SCOPUS:85172425561

SN - 0032-0889

VL - 193

SP - 1508

EP - 1526

JO - Plant Physiology

JF - Plant Physiology

IS - 2

ER -

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

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