scholarly journals Transcriptomic analysis with the progress of symbiosis in ‘crack-entry’ legume Arachis hypogaea highlights its contrast with ‘infection thread’ adapted legumes

2018 ◽  
Author(s):  
Kanchan Karmakar ◽  
Anindya Kundu ◽  
Ahsan Z Rizvi ◽  
Emeric Dubois ◽  
Dany Severac ◽  
...  
Keyword(s):  
Arachis Hypogaea ◽  
Root Nodule ◽  
Infection Thread ◽  
Symbiotic Genes ◽  
Cortical Cells ◽  
Transcriptional Dynamics ◽  
Infection Threads ◽  
Spread Of Infection ◽  
Molecular Framework ◽  
Nodule Symbiosis

ABSTRACTIn root-nodule symbiosis, rhizobial invasion and nodule organogenesis is host controlled. In most legumes, rhizobia enter through infection-threads and nodule primordium in the cortex is induced from a distance. But in dalbergoid legumes like Arachis hypogaea, rhizobia directly invade cortical cells through epidermal cracks to generate the primordia. Herein we report the transcriptional dynamics with the progress of symbiosis in A. hypogaea at 1dpi: invasion; 4dpi: nodule primordia; 8dpi: spread of infection in nodule-like structure; 12dpi: immature nodules containing rod-shaped rhizobia; and 21dpi: mature nodules with spherical symbiosomes. Expression of putative orthologue of symbiotic genes in ‘crack-entry’ legume A. hypogaea was compared with infection thread adapted model legumes. The contrasting features were (i) higher expression of receptors like LYR3, EPR3 as compared to canonical NFRs (ii) late induction of transcription factors like NIN, NSP2 and constitutive high expression of ERF1, EIN2, bHLH476 and (iii) induction of divergent pathogenesis responsive PR-1 genes. Additionally, symbiotic orthologues of SymCRK, FLOT4, ROP6, RR9, NOOT and SEN1 were not detectable and microsynteny analysis indicated the absence of RPG and DNF2 homologues in diploid parental genomes of A. hypogaea. The implications are discussed and a molecular framework that guide ‘crack-entry’ symbiosis in A. hypogaea is proposed.

scholarly journals Transcriptomic Analysis With the Progress of Symbiosis in ‘Crack-Entry’ Legume Arachis hypogaea Highlights Its Contrast With ‘Infection Thread’ Adapted Legumes

2019 ◽  
Vol 32 (3) ◽  
pp. 271-285 ◽  
Author(s):  
Kanchan Karmakar ◽  
Anindya Kundu ◽  
Ahsan Z Rizvi ◽  
Emeric Dubois ◽  
Dany Severac ◽  
...  
Keyword(s):  
Arachis Hypogaea ◽  
Root Nodule ◽  
Infection Thread ◽  
Cortical Cells ◽  
Nod Factor ◽  
Transcriptional Dynamics ◽  
Infection Threads ◽  
Spread Of Infection ◽  
Molecular Framework ◽  
Nodule Symbiosis

In root-nodule symbiosis, rhizobial invasion and nodule organogenesis is host controlled. In most legumes, rhizobia enter through infection threads and nodule primordium in the cortex is induced from a distance. But in dalbergoid legumes like Arachis hypogaea, rhizobia directly invade cortical cells through epidermal cracks to generate the primordia. Herein, we report the transcriptional dynamics with the progress of symbiosis in A. hypogaea at 1 day postinfection (dpi) (invasion), 4 dpi (nodule primordia), 8 dpi (spread of infection in nodule-like structure), 12 dpi (immature nodules containing rod-shaped rhizobia), and 21 dpi (mature nodules with spherical symbiosomes). Expression of putative ortholog of symbiotic genes in ‘crack entry’ legume A. hypogaea was compared with infection thread–adapted model legumes. The contrasting features were i) higher expression of receptors like LYR3 and EPR3 as compared with canonical Nod factor receptors, ii) late induction of transcription factors like NIN and NSP2 and constitutive high expression of ERF1, EIN2, bHLH476, and iii) induction of divergent pathogenesis-responsive PR-1 genes. Additionally, symbiotic orthologs of SymCRK, ROP6, RR9, SEN1, and DNF2 were not detectable and microsynteny analysis indicated the absence of a RPG homolog in diploid parental genomes of A. hypogaea. The implications are discussed and a molecular framework that guides crack-entry symbiosis in A. hypogaea is proposed.

scholarly journals Alfalfa Root Nodule Invasion Efficiency Is Dependent on Sinorhizobium melilotiPolysaccharides

2000 ◽  
Vol 182 (15) ◽  
pp. 4310-4318 ◽  
Author(s):  
Brett J. Pellock ◽  
Hai-Ping Cheng ◽  
Graham C. Walker
Keyword(s):  
Molecular Weight ◽  
Sinorhizobium Meliloti ◽  
Root Nodule ◽  
Fluorescent Protein ◽  
Infection Thread ◽  
Low Molecular Weight ◽  
Infection Threads ◽  
Green Fluorescent ◽  
K Antigen ◽  
Alfalfa Root

ABSTRACT The soil bacterium Sinorhizobium meliloti is capable of entering into a nitrogen-fixing symbiosis with Medicago sativa (alfalfa). Particular low-molecular-weight forms of certain polysaccharides produced by S. meliloti are crucial for establishing this symbiosis. Alfalfa nodule invasion by S. meliloti can be mediated by any one of three symbiotically important polysaccharides: succinoglycan, EPS II, or K antigen (also referred to as KPS). Using green fluorescent protein-labeled S. meliloti cells, we have shown that there are significant differences in the details and efficiencies of nodule invasion mediated by these polysaccharides. Succinoglycan is highly efficient in mediating both infection thread initiation and extension. However, EPS II is significantly less efficient than succinoglycan at mediating both invasion steps, and K antigen is significantly less efficient than succinoglycan at mediating infection thread extension. In the case of EPS II-mediated symbioses, the reduction in invasion efficiency results in stunted host plant growth relative to plants inoculated with succinoglycan or K-antigen-producing strains. Additionally, EPS II- and K-antigen-mediated infection threads are 8 to 10 times more likely to have aberrant morphologies than those mediated by succinoglycan. These data have important implications for understanding how S. meliloti polysaccharides are functioning in the plant-bacterium interaction, and models are discussed.

A shared gene drives lateral root development and root nodule symbiosis pathways in Lotus

Science ◽  
2019 ◽  
Vol 366 (6468) ◽  
pp. 1021-1023 ◽  
Author(s):  
Takashi Soyano ◽  
Yoshikazu Shimoda ◽  
Masayoshi Kawaguchi ◽  
Makoto Hayashi
Keyword(s):  
Root Development ◽  
Lateral Root ◽  
Root Nodule ◽  
Root Nodules ◽  
Lotus Japonicus ◽  
Cortical Cell ◽  
Cortical Cells ◽  
Lateral Root Development ◽  
Lateral Organ ◽  
Nodule Symbiosis

Legumes develop root nodules in symbiosis with nitrogen-fixing rhizobial bacteria. Rhizobia evoke cell division of differentiated cortical cells into root nodule primordia for accommodating bacterial symbionts. In this study, we show that NODULE INCEPTION (NIN), a transcription factor in Lotus japonicus that is essential for initiating cortical cell divisions during nodulation, regulates the gene ASYMMETRIC LEAVES 2-LIKE18/LATERAL ORGAN BOUNDARIES DOMAIN16a (ASL18/LBD16a). Orthologs of ASL18/LBD16a in nonlegume plants are required for lateral root development. Coexpression of ASL18a and the CCAAT box–binding protein Nuclear Factor-Y (NF-Y) subunits, which are also directly targeted by NIN, partially suppressed the nodulation-defective phenotype of L. japonicusdaphne mutants, in which cortical expression of NIN was attenuated. Our results demonstrate that ASL18a and NF-Y together regulate nodule organogenesis. Thus, a lateral root developmental pathway is incorporated downstream of NIN to drive nodule symbiosis.

scholarly journals The Noncanonical Heat Shock Protein PvNod22 Is Essential for Infection Thread Progression During Rhizobial Endosymbiosis in Common Bean

2019 ◽  
Vol 32 (8) ◽  
pp. 939-948
Author(s):  
Jonathan Rodríguez-López ◽  
Alejandrina Hernández López ◽  
Georgina Estrada-Navarrete ◽  
Federico Sánchez ◽  
Claudia Díaz-Camino
Keyword(s):  
Heat Shock ◽  
Heat Shock Protein ◽  
Common Bean ◽  
Root Nodule ◽  
Plant Immunity ◽  
Small Heat Shock Protein ◽  
Infection Thread ◽  
Nodule Development ◽  
Virus Induced Gene Silencing ◽  
Infection Threads

In the establishment of plant-rhizobial symbiosis, the plant hosts express nodulin proteins during root nodule organogenesis. A limited number of nodulins have been characterized, and these perform essential functions in root nodule development and metabolism. Most nodulins are expressed in the nodule and at lower levels in other plant tissues. Previously, we isolated Nodulin 22 (PvNod22) from a common bean (Phaseolus vulgaris L.) cDNA library derived from Rhizobium-infected roots. PvNod22 is a noncanonical, endoplasmic reticulum (ER)-localized, small heat shock protein that confers protection against oxidative stress when overexpressed in Escherichia coli. Virus-induced gene silencing of PvNod22 resulted in necrotic lesions in the aerial organs of P. vulgaris plants cultivated under optimal conditions, activation of the ER-unfolded protein response (UPR), and, finally, plant death. Here, we examined the expression of PvNod22 in common bean plants during the establishment of rhizobial endosymbiosis and its relationship with two cellular processes associated with plant immunity, the UPR and autophagy. In the RNA interference lines, numerous infection threads stopped their progression before reaching the cortex cell layer of the root, and nodules contained fewer nitrogen-fixing bacteroids. Collectively, our results suggest that PvNod22 has a nonredundant function during legume-rhizobia symbiosis associated with infection thread elongation, likely by sustaining protein homeostasis in the ER.

ELECTRON MICROSCOPY OF THE BACTEROIDS AND ROOT NODULES OF LUPINUS LUTEUS

1965 ◽  
Vol 11 (4) ◽  
pp. 721-725 ◽  
Author(s):  
D. C. Jordan ◽  
I. Grinyer
Keyword(s):  
Plant Cell ◽  
De Novo ◽  
Root Nodules ◽  
Cell Plate ◽  
Lupinus Luteus ◽  
Bacterial Cells ◽  
Intercellular Spaces ◽  
Cortical Cells ◽  
Infection Threads ◽  
Spread Of Infection

No intracellular infection threads were observed in ultrathin sections of young root nodules of lupine, although nodule bacteria could be found in the intercellular spaces between the root cortical cells. Evidence suggests that in certain instances the plant cell walls can be disrupted locally, allowing the bacteria to pass into cytoplasm of the host cell. The spread of infection may be initiated in this manner and extended by division of infected cells. No plant-produced enclosing membranes were present around bacteria in the intercellular spaces but such structures developed after the bacteria had entered the plant cell. Although the origin of these membranes is debatable, in the present work it appeared that they were formed de novo, perhaps in a manner akin to the development of the cell plate during cell division. Most of the bacterial cells possessed a wide subwall space lying between the bacterial cell wall and plasma membrane. Discontinuities present in the latter membrane may account for the ribosome-like material found in the subwall space.

scholarly journals Localization of acid phosphatase activity in the apoplast of root nodules of pea (Pisum sativum)

2011 ◽  
Vol 75 (1) ◽  
pp. 33-38 ◽  
Author(s):  
Marzena Sujkowska ◽  
Wojciech Borucki ◽  
Władysław Golinowski
Keyword(s):  
Enzyme Activity ◽  
Acid Phosphatase ◽  
Pisum Sativum ◽  
Root Nodule ◽  
Root Nodules ◽  
Outer Part ◽  
Inorganic Phosphorus ◽  
Infection Thread ◽  
Symbiotic Bacteria ◽  
Infection Threads

Changes in the activity of acid phosphatase (AcPase) in the apoplast of pea root nodule were investigated. The activity was determined using lead and cerium methods. The results indicated a following sequence of AcPase activity appearance during the development of the infection thread: 1) low AcPase activity appears in the outer part of cells of symbiotic bacteria; 2) bacteria show increased AcPase activity, and the enzyme activity appears in the thread walls; 3) activity exhibits also matrix of the infection thread; 4) bacteria just before their release from the infection threads show high AcPase activity; 5) AcPase activity ceases after bacteria transformation into bacteroids. The increase in bacterial AcPase activity may reflect a higher demand for inorganic phosphorus necessary for propagation of the bacteria within the infection threads and/or involved in bacteria release from the infection threads.

scholarly journals The monomeric GTPase RabA2 is required for progression and maintenance of membrane integrity of infection threads during root nodule symbiosis

2017 ◽  
Vol 93 (6) ◽  
pp. 549-562 ◽  
Author(s):  
Virginia Dalla Via ◽  
Soledad Traubenik ◽  
Claudio Rivero ◽  
O. Mario Aguilar ◽  
María Eugenia Zanetti ◽  
...  
Keyword(s):  
Root Nodule ◽  
Membrane Integrity ◽  
Root Nodule Symbiosis ◽  
Infection Threads ◽  
Nodule Symbiosis

scholarly journals The Ethylene Responsive Factor Required for Nodulation 1 (ERN1) Transcription Factor Is Required for Infection-Thread Formation in Lotus japonicus

2017 ◽  
Vol 30 (3) ◽  
pp. 194-204 ◽  
Author(s):  
Yasuyuki Kawaharada ◽  
Euan K. James ◽  
Simon Kelly ◽  
Niels Sandal ◽  
Jens Stougaard
Keyword(s):  
Transcription Factor ◽  
Root Nodule ◽  
Lotus Japonicus ◽  
Epidermal Cells ◽  
Infection Thread ◽  
Nod Factor ◽  
Infection Threads ◽  
Thread Formation ◽  
Ethylene Responsive Factor ◽  
Infection Thread Formation

Several hundred genes are transcriptionally regulated during infection-thread formation and development of nitrogen-fixing root nodules. We have characterized a set of Lotus japonicus mutants impaired in root-nodule formation and found that the causative gene, Ern1, encodes a protein with a characteristic APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription-factor domain. Phenotypic characterization of four ern1 alleles shows that infection pockets are formed but root-hair infection threads are absent. Formation of root-nodule primordia is delayed and no normal transcellular infection threads are found in the infected nodules. Corroborating the role of ERN1 (ERF Required for Nodulation1) in nodule organogenesis, spontaneous nodulation induced by an autoactive CCaMK and cytokinin–induced nodule primordia were not observed in ern1 mutants. Expression of Ern1 is induced in the susceptible zone by Nod factor treatment or rhizobial inoculation. At the cellular level, the pErn1:GUS reporter is highly expressed in root epidermal cells of the susceptible zone and in the cortical cells that form nodule primordia. The genetic regulation of this cellular expression pattern was further investigated in symbiotic mutants. Nod factor induction of Ern1 in epidermal cells was found to depend on Nfr1, Cyclops, and Nsp2 but was independent of Nin and Nf-ya1. These results suggest that ERN1 functions as a transcriptional regulator involved in the formation of infection threads and development of nodule primordia and may coordinate these two processes.

scholarly journals Turanose induced WOX5 restores symbiosis in the Medicago truncatula cytokinin perception mutant cre1

2019 ◽  
Author(s):  
Anindya Kundu ◽  
Firoz Molla ◽  
Maitrayee DasGupta
Keyword(s):  
Transcription Factor ◽  
Arachis Hypogaea ◽  
Root Nodule ◽  
Ectopic Expression ◽  
The Other ◽  
Sugar Signaling ◽  
Cytokinin Signaling ◽  
Signaling Axis ◽  
Auxin Accumulation ◽  
Nodule Symbiosis

ABSTRACTRhizobia-legume interaction recruits cytokinin-signaling that causes local auxin accumulation for the induction of nodule primordia in the cortex. Since sugar signaling can trigger auxin responses and regulate developmental processes, we explored whether sugar treatments could rescue cre1. Here we demonstrate that turanose, a non-metabolizable sucrose analogue can recover functional symbiosis in cytokinin perception mutant cre1. Additionally, turanose significantly upregulated the expression of WUSCHEL-related homeobox 5 (MtWOX5) which prompted us to check if ectopic expression of WOX5 could rescue cre1. Overexpression of WOX5 from Arachis hypogaea (AhWOX5), but not the intrinsic MtWOX5 could completely restore functional symbiosis in cre1 though both WOX5 (Mt and Ah) were functionally equivalent in inducing the expression of cytokinin inducible transcription factor Nodule Inception (NIN). Among the tested markers for cytokinin and auxin responses, significant differences were noted in the expression of IAA-Ala Resistant3 (MtIAR33), an auxin conjugate hydrolase. Turanose and AhWOX5 overexpression resulted in upregulation of MtIAR33 that further increased significantly in presence of rhizobia. On the other hand, MtIAR33 expression was unaffected in MtWOX5 overexpressed roots suggesting deconjugation driven auxin pool to be critical for rescuing symbiosis in cre1. We hypothesize a working model for sugar and WOX5 mediated rescue of symbiosis in cre1.One sentence summaryActivation of sugar-WOX5 signaling axis restores root nodule symbiosis in cytokinin perception mutant cre1

Cytoplasmic bridge formation in the nodule apex of actinorhizal root nodules

1999 ◽  
Vol 77 (9) ◽  
pp. 1351-1357 ◽  
Author(s):  
R Howard Berg
Keyword(s):  
Structural Changes ◽  
Root Nodules ◽  
Parenchyma Cell ◽  
Infection Process ◽  
Infection Thread ◽  
Cytoplasmic Bridge ◽  
Cortical Cells ◽  
Infection Threads ◽  
Related Plant ◽  
Cytoplasmic Bridges

High-pressure frozen - freeze-substituted actinorhizal root nodules of several distantly related plant genera were used to document the sequence of structural changes in cortical cells of the nodule apex that happened prior to their infection. The sequence of mobilization of the plant cell cytoplasm requisite to infection by Frankia was (i) penetration of the parenchyma cell vacuole by cytoplasmic strands, which contained microtubules; (ii) movement of the nucleus and other organelles (Golgi stacks, endoplasmic reticulum, mitochondria), involved later in growth of the infection thread, to the cell center on these strands; (iii) thickening of some of these strands generally located at midpoints of the wall, forming cytoplasmic bridges (preinfection threads); and (iv) infection of the cell by initiation of infection threads (containing Frankia) within the cytoplasmic bridges. The infection thread was caged in microtubules that were oriented along its axis, suggesting the cytoskeleton had a major role in the infection process, perhaps guiding the growth of the infection thread across the cell. The coalignment of cytoplasmic bridges, along several cells, towards the advancing microsymbiont suggested Frankia secretes a diffusible signal eliciting this host response.Key words: actinorhiza, cryofixation, development, infection, microtubules, symbiosis.

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