This Is an Author Produced Version of a Paper Published in SYMBIOSIS

This is an author produced version of a paper published in SYMBIOSIS. This paper has been peer-reviewed and is proof-corrected, but does not include the journal pagination.

Citation for the published paper: Eugenia E. Chaia, Luis G. Wall and Kerstin Huss-Danell. (2011) Life in soil by the actinorhizal root module endophyte Frankia: a review. Symbiosis. Volume: 51 Number: 3, pp 201-226. http://dx.doi.org/10.1007/s13199-010-0086-y

Access to the published version may require journal subscription. Published with permission from: Springer

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LIFE IN SOIL BY THE ACTINORHIZAL ROOT NODULE ENDOPHYTE FRANKIA . A REVIEW Eugenia E. Chaia 1, Luis G. Wall 2 and Kerstin Huss-Danell 3* CONTENTS Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia ABSTRACT

Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia

Frankia Keywords Frankia Frankia Abbreviations 1. Introduction

Frankia Frankia Frankia Frankia Frankia Frankia Alnus Frankia Frankia Alnus glutinosa Frankia Comptonia peregrina Frankia Frankia Frankia Frankia Frankia Frankia Alnus rubra Frankia Frankia glnII nif nif Frankia Frankia alni Frankia Alnus, Casuarina Myrica Frankia Dryas, Coriaria Datisca Ceanothus Ceanothus Frankia Frankia Frankia Parasponia . Alnus

Frankia Alnus Frankia Frankia Ceanothus Frankia Frankia Frankia Ceanothus Frankia in vitro Datisca glomerata

Figure 1. Discaria chacaye Discaria trinervis Discaria trinervis Discaria trinervis Frankia Discaria chacaye Frankia Dicsaria articulata

Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia in vitro Frankia Frankia Frankia i.e. Frankia Frankia Frankia Frankia Frankia Frankia 2. Morphology of Frankia Frankia Casuarina Allocasuarina Casuarina Allocasuarina Frankia Alnus Comptonia Myrica Frankia Frankia Frankia i.e

Frankia Frankia, Frankia in situ Frankia Frankia Frankia

Figure 2. Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Casuarina Allocasuarina Frankia Frankia Frankia Frankia Frankia Frankia

Frankia Table 1 Frankia Frankia Frankia Host family, Frankia Frankia Betulaceae Alnus Casuarinaceae Allocasuarina

Frankia Table 1 (continued) Host family, Frankia Frankia Casuarina Ceuthostoma h Gymnostoma Myricaceae Comptonia Myrica Morella nif Elaeagnaceae Elaeagnus

Frankia Table 1 (continued) Host family, Frankia Frankia Hippophaë Shepherdia Rhamnaceae Adolphia Ceanothus Colletia Discaria Kentrothamnus Retanilla Talguenea Trevoa Rosaceae Cercocarpus Chamaebatia Cowania Dryas

Frankia Table 1 (continued) Host family, Frankia Frankia Purshia Coriariaceae Coriaria Datiscaceae Datisca

Betula . Frankia Myrica Morella. Adolphia infesta Ceanothus infestus Discaria trinervis Ochetophila trinervis .

Frankia Table 2 Frankia Ceanothus americanus nif Discaria toumatou Ceanothus griseous Dryas Purshia tridentata drummondii Coriaria arborea C. plumosa Discaria trinervis a D. chacaye D. articulata Coriaria arborea C. plumosa Coriaria A.lnus glutinosa A. cordata A. viridis Elaeagnus pungens Casuarina equisetifolia Elaeagnus angustifolia Elaeagnus C. Ceanothus americanus americanus Colletia hystrix Talguenea quinquenervia Trevoa trinervis

Frankia Table 2 (continued) Alnus incana Myrica pensylvanica M. pensylvanica Myrica gale M. pensylvanica M. pensylvanica C. peregrina M. gale Comptonia peregrina Chamaebatia foliolosa Frankia Cercocarps ledifolius gln Purshia Shepherdia canadensis Frankia Alnus incana M. gale Myrica gale rrs S. canadensis Casuarina collina Elaeagnus Gymnostoma Ceanothus Frankia Frankia Elaeagnus Alnus nepalensis Frankia A. nepalensis Frankia Gymnostoma Gymnostoma Elaeagnus Casuarina Allocasuarina Casuarina equisetifolia Casuarina Allocasuarina C. cunninghamiana Gymnostoma Allocasuarina torulosa Elaeagnaceae Gymnostoma

Frankia Table 2 (continued) Gymnostoma Casuarina equisetifolia Ceanothus Frankia Chamaebatia Ceanothus Chamaebatia Ceanothus Ceanothus Frankia Ceanothus Casuarina equisetifolia rrn C. cunninghamiana nif Allocasuarina torulosa A. littoralis Casuarina esquisetifolia Frankia Alnus acuminata Frankia Frankia Rosaceae Frankia Ceanothus Datisca glomerata Discaria trinervis Ochetophila trinervis .

Frankia 3. Isolation of Frankia 3.1. Isolation from nodules Frankia Alnus glutinosa Frankia, Frankia Alnus glutinosa Frankia

3.2 Isolation of Frankia from soil Frankia Frankia ´ Cercocarpus, Ceanothus, Casuarina Myrica Frankia Cercocarpus montanus Frankia ´ Cercocarpus Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia 4. Measurements of N2 fixation by Frankia in soil Frankia Frankia Frankia Frankia

Frankia Frankia Frankia nif

5. Infection mechanisms and nodule development Frankia Frankia Frankia Frankia Frankia Casuarina glauca Frankia Frankia Frankia Frankia

6. Nodulation tests as a tool to study Frankia in soil 6.1 Qualitative tests Frankia Frankia Frankia Frankia Frankia Frankia Frankia 6.2 Quantitative tests Frankia Frankia Frankia Frankia

Frankia i.e. Frankia Frankia Frankia Alnus Frankia Myrica- Frankia Ceanothus Frankia Frankia Frankia Frankia Frankia 6.3 Factors influencing nodulation 6.3.1 Soil environment Frankia Frankia Ceanothus

Frankia 6.3.2 Plants Frankia Frankia Alnus, Myrica Shepherdia Alnus Myrica Shepherdia Shepherdia Alnus Myrica Alnus Alnus incana A. glutinosa A. rubra Alnus rubra>A. incana>A. glutinosa, A. rubra A. glutinosa Alnus glutinosa Frankia A. glutinosa Frankia, Frankia Alnus rubra A. rubra Frankia 6.3.3 Autoregulation Frankia´ ´

Frankia Table 3. Frankia

Soil properties Betula Frankia alni Frankia Frankia Betula Ceanothus Frankia Alnus glutinosa Frankia . Purshia Cowania Casuarina. Discaria Frankia Alnus Frankia Alnus Myrica Frankia Myrica Casuarina Frankia . Frankia Frankia Soil depth and altitude of sites Hippophaë. Purshia Cowania.

Frankia Table 3 (continued)

Myrica, Elaeagnus Alnus Frankia Elaeagnus Frankia Casuarina Frankia Alnus Temperature Ceanothus, Season Alnus Discaria Soils with host plants Casuarina Casuarina Frankia Frankia Alnus Frankia Ceanothus Soils without host plants Alnus Elaeagnus Condalia Alnus. Myrica Casuarina. Discaria Colletia Betula, Pinus Picea, Alnus Frankia Frankia . Frankia growth in the rhizosphere of non-host plants Betula Alnus, Frankia Betula, Poa Festuca Alphitonia Gymnostoma Pinus Alnus Rubus spectabilis Betula papyrifera

Frankia Table 3 (continued)

Soils lacking Frankia Alnus. Casuarina Alnus Frankia Allelochemicals

Frankia Casuarina , Frankia Frankia Casuarina Strain competition Frankia Frankia Alnus Frankia Interactions between Frankia and other soil organisms Frankia Frankia . Frankia Discaria Successional stage Hippophaë Alnus Myrica Dryas Shepherdia Frankia Alnus Myrica Frankia

Frankia Table 3 (continued)

Frankia Alnus Alnus Time without host plants Ceanothus Ceanothus. Alnus Alnus Dispersal Casuarina Frankia Casuarina Frankia Alnus Frankia Frankia Elaeagnus Frankia Frankia Frankia Alnus Elaeagnus Frankia. Frankia Casuarina . Soil reclamation Elaeagnus Shepherdia Frankia Frankia Casuarina Frankia Alnus Frankia Frankia Alnus Frankia Paxillus,

Frankia Table 3 (continued)

Discaria Alnus Frankia Alnus

Alnus Alnus Elaeagnus

Casuarina

Frankia

Frankia 6.3.4 Dispersal and survival of Frankia Frankia Frankia Frankia Frankia Alnus glutinosa Frankia Discaria trinervis D. americana Casuarina equisetifolia Alnus incana Frankia Casuarina cristata Frankia Frankia Frankia Alnus glutinosa Elaeagnus angustifolia Frankia Elaeagnus Frankia Frankia Frankia Frankia Casuarina equisetifolia Melopsittacus undulatus). Discaria trinervis Frankia Frankia Frankia Alnus rubra Frankia Alnus incana Frankia

Frankia Alnus Discaria trinervis D. trinervis Frankia Frankia Alnus incana Discaria trinervis 6.3.5 Plant and Frankia growth conditions e.g. Alnus glutinosa, A. incana Hippophaë rhamnoides Discaria trinervis Frankia Frankia

Frankia Frankia Frankia Frankia Frankia Frankia 7. Studies of Frankia in soil by DNA methods Frankia Frankia Frankia in situ e.g. Frankia Frankia 7.1 Quantitative studies Frankia Frankia Frankia Frankia Frankia Frankia Frankia . Frankia Frankia

Frankia 7.2 Genetic diversity Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Alnus Myrica Frankia Frankia Frankia Frankia Frankia, 8. Comparisons of nodulation tests and DNA studies in soil Elaeagnus Frankia Frankia nif Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia Alnus rubra Frankia Frankia Frankia Frankia Frankia Alnus.

Frankia Table 4 Frankia

9. Interactions between Frankia and other soil microorganisms 9.1 Bacteria Frankia Frankia Frankia Frankia -Frankia Frankia Casuarina equisetifolia Coriaria myrtifolia Elaeagnus angustifolia Alnus acuminata Frankia Frankia Frankia Frankia -Frankia Alnus glutinosa Casuarina glauca Elaeagnus angustifolia Pseudomonas cepacia Frankia Alnus rubra Streptomyces, Actinoplanes and Micromonospora Discaria trinervis Discaria trinervis Frankia Alnus glutinosa Pseudomonas Bacillus Frankia

Frankia Frankia Alnus Casuarina Elaeagnus Frankia Frankia Discaria trinervis Discaria trinervis Frankia Frankia Frankia

9.2 Mycorrhiza Alnus Ceanothus coeruleus Coriaria ruscifolia Discaria . Colletia hystrix Myrica cerifera Discaria trinervis Alnus Frankia Frankia Glomus Casuarina equisetifolia 10. Concluding remarks Frankia Frankia Frankia Frankia Frankia Frankia Frankia

Frankia . Frankia Frankia Frankia Frankia Frankia Alnus Frankia Frankia Frankia Frankia Frankia Frankia Frankia Frankia

11. Acknowledgements Frankia Frankia 12. References Frankia alni Frankia alni Frankia Frankia Frankia Frankia Ceanothus Actinobacterium Frankia Cortinarius helodes Gyrodon monticola Alnus acuminata

Frankia Alnus acuminata Frankia Frankia Alnus rubra Frankia Frankia Ceanothus griseous, Coriaria arborea, Coraria plumosa, Discaria toumatou Purshia tridentata Frankia Alnus rubra Frankia Casuarina Alnus Myrica Frankia Frankia Frankia Casuarina equisetifolia Melipsittacus undulatus Comptonia. Discaria trinervis Frankia Frankia Discaria trinervis Frankia Discaria Discaria trinervis Frankia

Frankia Datisca, Coriaria Alnus Frankia Frankia Frankia Frankia Alnus incana Myrica pensylvanica Frankia Frankia Adolphia infesta Frankia Discaria americana Casuarina Allocasuarina Alnus viridis Frankia Casuarina equisetifolia Austrocedrus Frankia Alnus glutinosa Frankia - Discaria trinervis Casuarina Elaeagnus Frankia Casuarina collina

Frankia Frankia Gymnostoma Alphitonia neocaledonica Hippophaë rhamnoides Alnus incana Alnus incana SymRK Frankia Frankia Alnus glutinosa, Casuarina glauca Elaeagnus angustifolia Elaeagnus Frankia Elaeagnus Frankia nif Frankia Alnus glutinosa Frankia Frankia Frankia Frankia Frankia Frankia Frankia Alnus glutinosa Alnus glutinosa Frankia Myrica gale Alnus incana Shepherdia canadensis Shepherdia, Alnus Myrica Frankia Frankia Alnus incana

Frankia Alnus Frankia Frankia Alnus Alnus Frankia Trifolium Rhizobium Frankia Ceanothus velutinus Ochetophila Frankia Alnus rubra Frankia Alnus nepalensis Frankia Pseudomonas cepacia Dryas Casuarina glauca Frankia ´ Frankia. Frankia Casuarina-Frankia Alnus rubra Frankia Paxillus involutus Alnus incana rugosa Frankia Frankia Frankia Frankia

Frankia Frankia Shepherdia, Alnus Myrica Kentrothamnus, Trevoa Coriaria Frankia Frankia Coriaria nepalensis Datisca cannabina Frankia Frankia Frankia Ceanothus Frankia Alnus Frankia Frankia Frankia Frankia Gymnostoma Elaeagnus Frankia . Frankia Gymnostoma Frankia Frankia Discaria toumatou Causarina equisetifolia Frankia

Frankia Frankia Frankia Frankia Ceanothus Discaria trinervis- Frankia Hippophae rhamnoides rhamnoides Frankia Frankia Frankia Frankia Alnus glutinosa Ceanothus Alnus glutinosa Alnus glutinosa Alnus glutinosa Alnus glutinosa Frankia Frankia Alnus glutinosa Frankia Ceanothus caeruleus Frankia Frankia

Frankia Frankia Pontoscolex corethurus Frankia Alnus incana Cowania Purshia Alnus glutinosa Frankia Ceanothus Frankia Frankia Enterobacter, Klebsiella Pseudomonas Frankia Alnus-acuminata-Frankia Frankia Frankia Casuarina Frankia In Frankia Frankia Casurina Frankia Myrica cerifera Frankia Glomus Casuarina equisetifolia Colletia, Retanilla, Talguenea Trevoa Frankia Frankia Betula pendula

Frankia Frankia Discaria trinervis Discaria trinervis-Frankia Frankia Micromonospora coriariae Coriaria myrtifolia Alnus acuminata. Frankia Casuarina equisetifolia Frankia In Discaria trinervis Frankia Discaria trinervis Frankia Alnus glutinosa Alnus glutinosa Frankia-Alnus Frankia Alnus glutinosa Frankia Alnus glutinosa Frankia Ceanothus Datisca glomerata

Frankia Elaeagnus commutata Shepherdia canadensis Frankia Alnus incana - Frankia Alnus incana Trifolium pratense In Alnus glutinosa Alnus incana Morella pensylvanica Myrica cerifera Frankia Ceanothus velutinus Ceanothus velutinus Frankia Alnus glutinosa Frankia Alnus glutinosa Frankia Alnus glutinosa . Frankia Myrica cerifera Frankia Frankia Alnus glutinosa Casuarina Myrica cerifera, Leucaena leucocephala Casuarina cunninghamiana Casuarina Frankia Casuarina cunninghamiana Casuarina cunninghamiana Frankia Frankia Casuarina

Frankia Alnus glutinosa Elaeagnus angustifolia Frankia.

Frankia