Literature DB >> 22989463

Identifying abnormalities in symbiotic development between Trifolium spp. and Rhizobium leguminosarum bv. trifolii leading to sub-optimal and ineffective nodule phenotypes.

V J Melino1, E A Drew, R A Ballard, W G Reeve, G Thomson, R G White, G W O'Hara.   

Abstract

BACKGROUND AND AIMS: Legumes overcome nitrogen limitations by entering into a mutualistic symbiosis with N(2)-fixing bacteria (rhizobia). Fully compatible associations (effective) between Trifolium spp. and Rhizobium leguminosarum bv. trifolii result from successful recognition of symbiotic partners in the rhizosphere, root hair infection and the formation of nodules where N(2)-fixing bacteroids reside. Poorly compatible associations can result in root nodule formation with minimal (sub-optimal) or no (ineffective) N(2)-fixation. Despite the abundance and persistence of strains in agricultural soils which are poorly compatible with the commercially grown clover species, little is known of how and why they fail symbiotically. The aims of this research were to determine the morphological aberrations occurring in sub-optimal and ineffective clover nodules and to determine whether reduced bacteroid numbers or reduced N(2)-fixing activity is the main cause for the Sub-optimal phenotype.
METHODS: Symbiotic effectiveness of four Trifolium hosts with each of four R. leguminosarum bv. trifolii strains was assessed by analysis of plant yields and nitrogen content; nodule yields, abundance, morphology and internal structure; and bacteroid cytology, quantity and activity. KEY
RESULTS: Effective nodules (Nodule Function 83-100 %) contained four developmental zones and N(2)-fixing bacteroids. In contrast, Sub-optimal nodules of the same age (Nodule Function 24-57 %) carried prematurely senescing bacteroids and a small bacteroid pool resulting in reduced shoot N. Ineffective-differentiated nodules carried bacteroids aborted at stage 2 or 3 in differentiation. In contrast, bacteroids were not observed in Ineffective-vegetative nodules despite the presence of bacteria within infection threads.
CONCLUSIONS: Three major responses to N(2)-fixation incompatibility between Trifolium spp. and R. l. trifolii strains were found: failed bacterial endocytosis from infection threads into plant cortical cells, bacteroid differentiation aborted prematurely, and a reduced pool of functional bacteroids which underwent premature senescence. We discuss possible underlying genetic causes of these developmental abnormalities and consider impacts on N(2)-fixation of clovers.

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Year:  2012        PMID: 22989463      PMCID: PMC3503493          DOI: 10.1093/aob/mcs206

Source DB:  PubMed          Journal:  Ann Bot        ISSN: 0305-7364            Impact factor:   4.357


  27 in total

1.  The cytology of bacteroids from root nodules of subterranean clover (Trifolium subterraneum L.).

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Journal:  J Gen Microbiol       Date:  1955-12

Review 2.  Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation.

Authors:  Janet I Sprent
Journal:  New Phytol       Date:  2007       Impact factor: 10.151

3.  Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules.

Authors:  J Vasse; F de Billy; S Camut; G Truchet
Journal:  J Bacteriol       Date:  1990-08       Impact factor: 3.490

4.  16S ribosomal DNA amplification for phylogenetic study.

Authors:  W G Weisburg; S M Barns; D A Pelletier; D J Lane
Journal:  J Bacteriol       Date:  1991-01       Impact factor: 3.490

5.  A low-viscosity epoxy resin embedding medium for electron microscopy.

Authors:  A R Spurr
Journal:  J Ultrastruct Res       Date:  1969-01

6.  The Rhizobium leguminosarum biovar trifolii ANU794 induces novel developmental responses on the subterranean clover cultivar Woogenellup.

Authors:  Angela Carmen Morris; Michael Anthony Djordjevic
Journal:  Mol Plant Microbe Interact       Date:  2006-05       Impact factor: 4.171

7.  Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids.

Authors:  J Prell; J P White; A Bourdes; S Bunnewell; R J Bongaerts; P S Poole
Journal:  Proc Natl Acad Sci U S A       Date:  2009-07-13       Impact factor: 11.205

8.  Host-specific regulation of symbiotic nitrogen fixation in Rhizobium leguminosarum biovar trifolii.

Authors:  Simon H Miller; Rachel M Elliot; John T Sullivan; Clive W Ronson
Journal:  Microbiology       Date:  2007-09       Impact factor: 2.777

Review 9.  What determines the efficiency of N(2)-fixing Rhizobium-legume symbioses?

Authors:  Jason J Terpolilli; Graham A Hood; Philip S Poole
Journal:  Adv Microb Physiol       Date:  2012       Impact factor: 3.517

10.  Complete genome sequence of Rhizobium leguminosarum bv. trifolii strain WSM1325, an effective microsymbiont of annual Mediterranean clovers.

Authors:  Wayne Reeve; Graham O'Hara; Patrick Chain; Julie Ardley; Lambert Bräu; Kemanthi Nandesena; Ravi Tiwari; Alex Copeland; Matt Nolan; Cliff Han; Thomas Brettin; Miriam Land; Galina Ovchinikova; Natalia Ivanova; Konstantinos Mavromatis; Victor Markowitz; Nikos Kyrpides; Vanessa Melino; Matthew Denton; Ron Yates; John Howieson
Journal:  Stand Genomic Sci       Date:  2010-06-15
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  12 in total

1.  A Sulfoglycolytic Entner-Doudoroff Pathway in Rhizobium leguminosarum bv. trifolii SRDI565.

Authors:  Jinling Li; Ruwan Epa; Nichollas E Scott; Dominik Skoneczny; Mahima Sharma; Alexander J D Snow; James P Lingford; Ethan D Goddard-Borger; Gideon J Davies; Malcolm J McConville; Spencer J Williams
Journal:  Appl Environ Microbiol       Date:  2020-07-20       Impact factor: 4.792

2.  The direct effects of plant polyploidy on the legume-rhizobia mutualism.

Authors:  Nicole J Forrester; Tia-Lynn Ashman
Journal:  Ann Bot       Date:  2018-02-12       Impact factor: 4.357

Review 3.  Structure and Development of the Legume-Rhizobial Symbiotic Interface in Infection Threads.

Authors:  Anna V Tsyganova; Nicholas J Brewin; Viktor E Tsyganov
Journal:  Cells       Date:  2021-04-29       Impact factor: 6.600

4.  Optimizing Rhizobium-legume symbioses by simultaneous measurement of rhizobial competitiveness and N2 fixation in nodules.

Authors:  Marcela A Mendoza-Suárez; Barney A Geddes; Carmen Sánchez-Cañizares; Ricardo H Ramírez-González; Charlotte Kirchhelle; Beatriz Jorrin; Philip S Poole
Journal:  Proc Natl Acad Sci U S A       Date:  2020-04-21       Impact factor: 12.779

5.  The Regulatory Protein RosR Affects Rhizobium leguminosarum bv. trifolii Protein Profiles, Cell Surface Properties, and Symbiosis with Clover.

Authors:  Kamila Rachwał; Aleksandra Boguszewska; Joanna Kopcińska; Magdalena Karaś; Marek Tchórzewski; Monika Janczarek
Journal:  Front Microbiol       Date:  2016-08-23       Impact factor: 5.640

6.  Host-dependent symbiotic efficiency of Rhizobium leguminosarum bv. trifolii strains isolated from nodules of Trifolium rubens.

Authors:  Monika Marek-Kozaczuk; Sylwia Wdowiak-Wróbel; Michał Kalita; Mykhaylo Chernetskyy; Kamil Deryło; Marek Tchórzewski; Anna Skorupska
Journal:  Antonie Van Leeuwenhoek       Date:  2017-08-08       Impact factor: 2.271

7.  Genome sequence of the Trifolium rueppellianum -nodulating Rhizobium leguminosarum bv. trifolii strain WSM2012.

Authors:  Wayne Reeve; Vanessa Melino; Julie Ardley; Rui Tian; Sofie De Meyer; Jason Terpolilli; Ravi Tiwari; Ronald Yates; Graham O'Hara; John Howieson; Mohamed Ninawi; Brittany Held; David Bruce; Chris Detter; Roxanne Tapia; Cliff Han; Chia-Lin Wei; Marcel Huntemann; James Han; I-Min Chen; Konstantinos Mavromatis; Victor Markowitz; Ernest Szeto; Natalia Ivanova; Natalia Mikhailova; Ioanna Pagani; Amrita Pati; Lynne Goodwin; Tanja Woyke; Nikos Kyrpides
Journal:  Stand Genomic Sci       Date:  2013-12-15

8.  Genome sequence of the clover-nodulating Rhizobium leguminosarum bv. trifolii strain SRDI565.

Authors:  Wayne Reeve; Elizabeth Drew; Ross Ballard; Vanessa Melino; Rui Tian; Sofie De Meyer; Lambert Brau; Mohamed Ninawi; Hazuki Teshima; Lynne Goodwin; Patrick Chain; Konstantinos Liolios; Amrita Pati; Konstantinos Mavromatis; Natalia Ivanova; Victor Markowitz; Tanja Woyke; Nikos Kyrpides
Journal:  Stand Genomic Sci       Date:  2013-12-15

9.  Genome sequence of the clover-nodulating Rhizobium leguminosarum bv. trifolii strain SRDI943.

Authors:  Wayne Reeve; Elizabeth Drew; Ross Ballard; Vanessa Melino; Rui Tian; Sofie De Meyer; Lambert Brau; Mohamed Ninawi; Hajnalka Daligault; Karen Davenport; Tracy Erkkila; Lynne Goodwin; Wei Gu; Christine Munk; Hazuki Teshima; Yan Xu; Patrick Chain; Nikos Kyrpides
Journal:  Stand Genomic Sci       Date:  2013-12-15

10.  Genome sequence of the clover-nodulating Rhizobium leguminosarum bv. trifolii strain TA1.

Authors:  Wayne Reeve; Rui Tian; Sofie De Meyer; Vanessa Melino; Jason Terpolilli; Julie Ardley; Ravi Tiwari; John Howieson; Ronald Yates; Graham O'Hara; Mohamed Ninawi; Hazuki Teshima; David Bruce; Chris Detter; Roxanne Tapia; Cliff Han; Chia-Lin Wei; Marcel Huntemann; James Han; I-Min Chen; Konstantinos Mavromatis; Victor Markowitz; Natalia Ivanova; Galina Ovchinnikova; Ioanna Pagani; Amrita Pati; Lynne Goodwin; Sam Pitluck; Tanja Woyke; Nikos Kyrpides
Journal:  Stand Genomic Sci       Date:  2013-12-15
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