The Root Hair “Infectome” of <i>Medicago truncatula</i> Uncovers Changes in Cell Cycle Genes and Reveals a Requirement for Auxin Signaling in Rhizobial Infection

Breakspear, Andrew; Liu, Cheng-Wu; Roy, Sonali; Stacey, Nicola; Rogers, Christian; Trick, Martin; Morieri, Giulia; Mysore, Kirankumar S.; Wen, Jiangqi; Oldroyd, Giles; Downie, J. Allan; Murray, Jeremy D.

doi:10.1105/tpc.114.133496

Cited by 299 publications

(463 citation statements)

References 167 publications

(177 reference statements)

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“…In agreement with Breakspear et al (2014), we observed Nod factor-induced expression of the strigolactone biosynthetic genes DWARF27 (contig_16099_1) and MAX1 (Medtr3g104560). Notably, the SL biosynthetic pathway is partially redundant with the pathway leading to ABA biosynthesis, suggesting that ABA biosynthesis is also up-regulated (Supplemental Fig.…”

Section: Et Regulates Multiple Hormone Biosynthetic Pathwayssupporting

confidence: 74%

“…FH8 overexpression in Arabidopsis causes root hair swelling and branching similar to Nod factors in legumes. Root hair curling and infection are also associated with changes in the microtubule cytoskeleton, and b-tubulins, which are cytoskeletal proteins, have been shown to be up-regulated in root hairs (Timmers, 2008;Breakspear et al, 2014; Perrine-Walker et al, 2014). We Sorin et al (2014).…”

Section: Early Induction Of Genes Involved In Polar Root Hair Growthmentioning

confidence: 99%

“…Two genes up-regulated in the 3-to 6-h interval are homologs of Arabidopsis Formin-Like8 (AtFH8) and Abscisic Acid Insensitive-Like (ABIL), genes directly linked to actin nucleation and severing (Yi et al, 2005). ABIL functions in the SCAR/WAVE complex that regulates the actin cytoskeleton in tip-growing cells and during infection thread progression in legumes (Yokota et al, 2009;Miyahara et al, 2010;Hossain et al, 2012) and was recently observed to be up-regulated in root hairs undergoing infection (Breakspear et al, 2014). By contrast, AtFH8 is a formin, and a role for formins in symbiotic infection has not yet been reported.…”

Section: Early Induction Of Genes Involved In Polar Root Hair Growthmentioning

confidence: 99%

“…Several array-based studies have characterized transcriptional changes occurring during nodule formation (El Yahyaoui et al, 2004;Mitra et al, 2004;Lohar et al, 2006;Benedito et al, 2008;Breakspear et al, 2014). Most studies analyzed relatively late time points and were limited by their incomplete representation of plant genes, reduced sensitivity, and inability to reliably discriminate close paralogs.…”

mentioning

confidence: 99%

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Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

et al. 2015

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The legume-rhizobium symbiosis is initiated through the activation of the Nodulation (Nod) factor-signaling cascade, leading to a rapid reprogramming of host cell developmental pathways. In this work, we combine transcriptome sequencing with molecular genetics and network analysis to quantify and categorize the transcriptional changes occurring in roots of Medicago truncatula from minutes to days after inoculation with Sinorhizobium medicae. To identify the nature of the inductive and regulatory cues, we employed mutants with absent or decreased Nod factor sensitivities (i.e. Nodulation factor perception and Lysine motif domain-containing receptor-like kinase3, respectively) and an ethylene (ET)-insensitive, Nod factor-hypersensitive mutant (sickle). This unique data set encompasses nine time points, allowing observation of the symbiotic regulation of diverse biological processes with high temporal resolution. Among the many outputs of the study is the early Nod factorinduced, ET-regulated expression of ET signaling and biosynthesis genes. Coupled with the observation of massive transcriptional derepression in the ET-insensitive background, these results suggest that Nod factor signaling activates ET production to attenuate its own signal. Promoter:b-glucuronidase fusions report ET biosynthesis both in root hairs responding to rhizobium as well as in meristematic tissue during nodule organogenesis and growth, indicating that ET signaling functions at multiple developmental stages during symbiosis. In addition, we identified thousands of novel candidate genes undergoing Nod factor-dependent, ET-regulated expression. We leveraged the power of this large data set to model Nod factor-and ET-regulated signaling networks using MERLIN, a regulatory network inference algorithm. These analyses predict key nodes regulating the biological process impacted by Nod factor perception. We have made these results available to the research community through a searchable online resource.

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Section: Et Regulates Multiple Hormone Biosynthetic Pathwayssupporting

confidence: 74%

Section: Early Induction Of Genes Involved In Polar Root Hair Growthmentioning

confidence: 99%

Section: Early Induction Of Genes Involved In Polar Root Hair Growthmentioning

confidence: 99%

mentioning

confidence: 99%

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Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

et al. 2015

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“…This is also the case of DRM-associated proteins which accounted for 30% of the AM-responsive proteins. Among them, substantiating similarities in the development of both fungal and bacterial symbioses (Bapaume and Reinhardt 2012), the AM-induced lysine/ histidine transporter, MtAnn1 and flotillin-like 4 (FLOT4) also play role in rhizobial symbiosis (Vincill et al 2005;Breakspear et al 2014). In support of the importance of membrane microdomain-associated proteins in symbiotic relationships, the lysine/histidine transporter and FLOT4 have a continuing presence on the symbiosome membrane (Vincill et al 2005;Clarke et al 2015), and plants silenced for the DRMassociated FLOT4 protein form a reduced number of nodules that do not fix nitrogen efficiently (Haney and Long 2010).…”

Section: Analysis Of the Am-responsive Proteinsmentioning

confidence: 87%

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

Aloui¹,

Recorbet²,

Lemaître‐Guillier³

et al. 2017

Mycorrhiza

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In arbuscular mycorrhizal (AM) roots, the plasma membrane (PM) of the host plant is involved in all developmental stages of the symbiotic interaction, from initial recognition to intracellular accommodation of intra-radical hyphae and arbuscules. Although the role of the PM as the agent for cellular morphogenesis and nutrient exchange is especially accentuated in endosymbiosis, very little is known regarding the PM protein composition of mycorrhizal roots. To obtain a global overview at the proteome level of the host PM proteins as modified by symbiosis, we performed a comparative protein profiling of PM fractions from Medicago truncatula roots either inoculated or not with the AM fungus Rhizophagus irregularis. PM proteins were isolated from root microsomes using an optimized discontinuous sucrose gradient; their subsequent analysis by liquid chromatography followed by mass spectrometry (MS) identified 674 proteins. Cross-species sequence homology searches combined with MS-based quantification clearly confirmed enrichment in PM-associated proteins and depletion of major microsomal contaminants. Changes in protein amounts between the PM proteomes of mycorrhizal and non-mycorrhizal roots were monitored further by spectral counting. This workflow identified a set of 82 mycorrhiza-responsive proteins that provided insights into the plant PM response to mycorrhizal symbiosis. Among them, the association of one third of the mycorrhiza-responsive proteins with detergent-resistant membranes pointed at partitioning to PM microdomains. The PM-associated proteins responsive to mycorrhization also supported host plant control of sugar uptake to limit fungal colonization, and lipid turnover events in the PM fraction of symbiotic roots. Because of the depletion upon symbiosis of proteins mediating the replacement of phospholipids by phosphorus-free lipids in the plasmalemma, we propose a role of phosphate nutrition in the PM composition of mycorrhizal roots.

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A snapshot of functional genetic studies inMedicago truncatula

Kang¹,

Li²,

Sinharoy³

et al. 2019

The Model Legume Medicago Truncatula

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In the current context of food security, increase of plant protein production in a sustainable manner represents one of the major challenges of agronomic research, which could be partially resolved by increased cultivation of legume crops. Medicago truncatula is now a well-established model for legume genomic and genetic studies. With the establishment of genomics tools and mutant populations in M. truncatula, it has become an important resource to answer some of the basic biological questions related to plant development and stress tolerance. This review has an objective to overview a decade of genetic studies in this model plant from generation of mutant populations to nowadays. To date, the three biological fields, which have been extensively studied in M. truncatula, are the symbiotic nitrogen fixation, the seed development, and the abiotic stress tolerance, due to their significant agronomic impacts. In this review, we summarize functional genetic studies related to these three major biological fields. We integrated analyses of a nearly exhaustive list of genes into their biological contexts in order to provide an overview of the forefront research advances in this important legume model plant.

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The Root Hair “Infectome” of Medicago truncatula Uncovers Changes in Cell Cycle Genes and Reveals a Requirement for Auxin Signaling in Rhizobial Infection

Cited by 299 publications

References 167 publications

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

A snapshot of functional genetic studies inMedicago truncatula

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