Journal Article

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

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

in Annals of Botany

Published on behalf of The Annals of Botany Company

Volume 110, issue 8, pages 1559-1572
Published in print December 2012 | ISSN: 0305-7364
Published online September 2012 | e-ISSN: 1095-8290 | DOI: http://dx.doi.org/10.1093/aob/mcs206
Identifying abnormalities in symbiotic development between Trifolium spp. and Rhizobium leguminosarum bv. trifolii leading to sub-optimal and ineffective nodule phenotypes

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  • Ecology and Conservation
  • Evolutionary Biology
  • Plant Sciences and Forestry

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Background and Aims

Legumes overcome nitrogen limitations by entering into a mutualistic symbiosis with N2-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 N2-fixing bacteroids reside. Poorly compatible associations can result in root nodule formation with minimal (sub-optimal) or no (ineffective) N2-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 N2-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 N2-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 N2-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 N2-fixation of clovers.

Keywords: Trifolium subterraneum; T. purpureum; T. polymorphum; Rhizobium; symbiosis; bacteroid; clover; compatibility; effective; nitrogen fixation; nodule morphology

Journal Article.  7837 words.  Illustrated.

Subjects: Ecology and Conservation ; Evolutionary Biology ; Plant Sciences and Forestry

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