Paper · 2021 · Frontiers in Microbiology

Root Nodule Rhizobia From Undomesticated Shrubs of the Dry Woodlands of Southern Africa Can Nodulate Angolan Teak Pterocarpus angolensis, an Important Source of Timber

Wiebke Bünger; Abhijit Sarkar; Jann Lasse Grönemeyer; et al.

11
claims
18
verbatim quotes
10
citations
3
research areas
✓
Open access · cc-by

Abstract

Pterocarpus angolensis , a leguminous tree native to the dry woodlands of Southern Africa, provides valuable timber, but is threatened by land conversion and overharvesting while showing limited natural regeneration. Nitrogen-fixing root nodule symbionts that could improve establishment of young seedlings have not yet been described. Therefore, we investigated the ability of P. angolensis to form nodules with a diverse range of rhizobia. In drought-prone areas under climate change with higher temperatures, inoculants that are heat-tolerant and adapted to these conditions are likely to be of advantage. Sources of bacterial isolates were roots of P. angolensis from nurseries in the Kavango region, other shrubs from this area growing near Pterocarpus such as Indigofera rautanenii , Desmodium barbatum , Chamaecrista sp., or shrubs from drought-prone areas in Namaqualand ( Wiborgia monoptera , Leobordea digitata ) or Kalahari ( Indigofera alternans ). Only slight protrusions were observed on P. angolensis roots, from which a non-nodulating Microbacterium sp. was isolated. Rhizobia that were isolated from nodules of other shrubs were affiliated to Bradyrhizobium ripae WR4 T , Bradyrhizobium spp. (WR23/WR74/WR93/WR96), or Ensifer/Mesorhizobium (WR41/WR52). As many plant growth-promoting rhizobacteria (PGPR), nodule isolates produced siderophores and solubilized phosphate. Among them, only the Bradyrhizobium strains nodulated P. angolensis under controlled conditions in the laboratory. Isolates were further characterized by multilocus sequence analysis and were found to be distant from known Bradyrhizobium species. Among additional reference species tested for nodulation on P. angolensis , Bradyrhizobium vignae 7-2 T and Bradyrhizobium namibiense 5-10 T from the Kavango region of Namibia as well as Bradyrhizobium elkanii LMG6234 T and Bradyrhizobium yuanmingense LMG21728 T induced nitrogen-fixing nodules, while Bradyrhizobium diazoefficiens USDA110 T and Bradyrhizobium tropiciagri SEMIA6148 T did not. This suggests a broad microsymbiont range from Bradyrhizobium japonicum and B. elkanii lineages. Phylogenetic analysis of nodC genes indicated that nodulating bradyrhizobia did not belong to a specific symbiovar. Also, for I. rautanenii and Wiborgia , nodule isolates B. ripae WR4 T or Mesorhizobium sp. WR52, respectively, were authenticated. Characterization of symbionts inducing effective root nodules in P. angolensis and other shrubs from Subsahara Africa (SSA) give insights in their symbiotic partners for the first time and might help in future to develop bioinoculants for young seedlings in nurseries, and for reforestation efforts in Southern Africa.

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The text the model read, with the source record’s inline markup (italics, sub- and superscripts) rendered and its character entities decoded; quote offsets refer to the raw text.

Claims 11

Observationobservedoriginal resultmeasured

Claim · model-written summary

P. angolensis roots had only slight protrusions and yielded a non-nodulating Microbacterium sp.

Taxon
P. angolensisPterocarpus angolensise0
Interactor
Microbacterium sp.Microbacteriume0symbiont
Outcome
slight protrusionse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pterocarpus angolensis
Pterocarpus angolensis · TaxonSAplants · CC BY-SA 4.0 · Wikimedia Commons ↗
Microbacterium
Microbacterium · Interactor · picture from its Wikimedia Commons categoryAgricultural Research Service (NRRL)Culture Collection · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Only slight protrusions were observed on P. angolensis roots, from which a non-nodulating Microbacterium sp. was isolated”

✓ located verbatim in the source · abstract, characters 961–1082 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Only Bradyrhizobium strains among the shrub isolates nodulated P. angolensis in the laboratory.

Taxon
P. angolensisPterocarpus angolensise0
Treatment
Bradyrhizobium strainse0
Interactor
Bradyrhizobium strainse0symbiont
Outcome
nodulated P. angolensise0
Setting
laboratorye0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pterocarpus angolensis
Pterocarpus angolensis · TaxonSAplants · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“only the Bradyrhizobium strains nodulated P. angolensis under controlled conditions in the laboratory”

✓ located verbatim in the source · abstract, characters 1400–1501 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Bradyrhizobium vignae 7-2 T induced nitrogen-fixing nodules on P. angolensis.

Taxon
Pterocarpus angolensisPterocarpus angolensist0
Treatment
Bradyrhizobium vignae 7-2 Te0
Interactor
Bradyrhizobium vignae 7-2 TBradyrhizobium vignaee0symbiont
Outcome
nitrogen-fixing nodulese0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pterocarpus angolensis
Pterocarpus angolensis · TaxonSAplants · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Bradyrhizobium vignae 7-2 T and Bradyrhizobium namibiense 5-10 T from the Kavango region of Namibia as well as Bradyrhizobium elkanii LMG6234 T and Bradyrhizobium yuanmingense LMG21728 T induced nitrogen-fixing nodules”

✓ located verbatim in the source · abstract, characters 1711–1929 · show in text ↑
t0

“Pterocarpus angolensis”

✓ located verbatim in the source · title, characters 114–136 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Bradyrhizobium namibiense 5-10 T induced nitrogen-fixing nodules.

Taxon
Pterocarpus angolensisPterocarpus angolensist0
Treatment
Bradyrhizobium namibiense 5-10 Te0
Interactor
Bradyrhizobium namibiense 5-10 TBradyrhizobium namibiensee0symbiont
Outcome
nitrogen-fixing nodulese0
Setting
Kavango region of Namibiae0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pterocarpus angolensis
Pterocarpus angolensis · TaxonSAplants · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Bradyrhizobium vignae 7-2 T and Bradyrhizobium namibiense 5-10 T from the Kavango region of Namibia as well as Bradyrhizobium elkanii LMG6234 T and Bradyrhizobium yuanmingense LMG21728 T induced nitrogen-fixing nodules”

✓ located verbatim in the source · abstract, characters 1711–1929 · show in text ↑
t0

“Pterocarpus angolensis”

✓ located verbatim in the source · title, characters 114–136 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Bradyrhizobium elkanii LMG6234 T induced nitrogen-fixing nodules.

Taxon
Pterocarpus angolensisPterocarpus angolensist0
Treatment
Bradyrhizobium elkanii LMG6234 Te0
Interactor
Bradyrhizobium elkanii LMG6234 TBradyrhizobium elkaniie0symbiont
Outcome
nitrogen-fixing nodulese0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pterocarpus angolensis
Pterocarpus angolensis · TaxonSAplants · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Bradyrhizobium vignae 7-2 T and Bradyrhizobium namibiense 5-10 T from the Kavango region of Namibia as well as Bradyrhizobium elkanii LMG6234 T and Bradyrhizobium yuanmingense LMG21728 T induced nitrogen-fixing nodules”

✓ located verbatim in the source · abstract, characters 1711–1929 · show in text ↑
t0

“Pterocarpus angolensis”

✓ located verbatim in the source · title, characters 114–136 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Bradyrhizobium yuanmingense LMG21728 T induced nitrogen-fixing nodules.

Taxon
Pterocarpus angolensisPterocarpus angolensist0
Treatment
Bradyrhizobium yuanmingense LMG21728 Te0
Interactor
Bradyrhizobium yuanmingense LMG21728 TBradyrhizobium yuanmingensee0symbiont
Outcome
nitrogen-fixing nodulese0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pterocarpus angolensis
Pterocarpus angolensis · TaxonSAplants · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Bradyrhizobium vignae 7-2 T and Bradyrhizobium namibiense 5-10 T from the Kavango region of Namibia as well as Bradyrhizobium elkanii LMG6234 T and Bradyrhizobium yuanmingense LMG21728 T induced nitrogen-fixing nodules”

✓ located verbatim in the source · abstract, characters 1711–1929 · show in text ↑
t0

“Pterocarpus angolensis”

✓ located verbatim in the source · title, characters 114–136 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Bradyrhizobium diazoefficiens USDA110 T failed to induce nodules.

Taxon
Pterocarpus angolensisPterocarpus angolensist0
Treatment
Bradyrhizobium diazoefficiens USDA110 Te0
Interactor
Bradyrhizobium diazoefficiens USDA110 TBradyrhizobium diazoefficiense0symbiont
Outcome
did note0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pterocarpus angolensis
Pterocarpus angolensis · TaxonSAplants · CC BY-SA 4.0 · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Bradyrhizobium diazoefficiens USDA110 T and Bradyrhizobium tropiciagri SEMIA6148 T did not”

✓ located verbatim in the source · abstract, characters 1937–2027 · show in text ↑
t0

“Pterocarpus angolensis”

✓ located verbatim in the source · title, characters 114–136 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Bradyrhizobium tropiciagri SEMIA6148 T failed to induce nodules.

Taxon
Pterocarpus angolensisPterocarpus angolensist0
Treatment
Bradyrhizobium tropiciagri SEMIA6148 Te0
Interactor
Bradyrhizobium tropiciagri SEMIA6148 TBradyrhizobium tropiciagrie0symbiont
Outcome
did note0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pterocarpus angolensis
Pterocarpus angolensis · TaxonSAplants · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Bradyrhizobium diazoefficiens USDA110 T and Bradyrhizobium tropiciagri SEMIA6148 T did not”

✓ located verbatim in the source · abstract, characters 1937–2027 · show in text ↑
t0

“Pterocarpus angolensis”

✓ located verbatim in the source · title, characters 114–136 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Nodulating bradyrhizobia did not belong to a specific symbiovar.

Taxon
Pterocarpus angolensisPterocarpus angolensist0
Interactor
bradyrhizobiae0symbiont
Gene
nodC genese0
Outcome
did not belong to a specific symbiovare0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pterocarpus angolensis
Pterocarpus angolensis · TaxonSAplants · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Phylogenetic analysis of nodC genes indicated that nodulating bradyrhizobia did not belong to a specific symbiovar”

✓ located verbatim in the source · abstract, characters 2126–2240 · show in text ↑
t0

“Pterocarpus angolensis”

✓ located verbatim in the source · title, characters 114–136 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

B. ripae WR4 T was authenticated as a nodule isolate for I. rautanenii.

Taxon
I. rautaneniiIndigofera rautaneniie0
Interactor
B. ripae WR4 TBradyrhizobium ripaee0symbiont
Outcome
nodule isolatese0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Indigofera rautanenii
Indigofera rautanenii · TaxonDave U · CC BY-SA 4.0 · iNaturalist ↗

Verbatim

e0

“for I. rautanenii and Wiborgia , nodule isolates B. ripae WR4 T or Mesorhizobium sp. WR52, respectively, were authenticated”

✓ located verbatim in the source · abstract, characters 2248–2371 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Mesorhizobium sp. WR52 was authenticated as a nodule isolate for Wiborgia.

Taxon
WiborgiaWiborgiae0
Interactor
Mesorhizobium sp. WR52e0symbiont
Outcome
nodule isolatese0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Wiborgia
Wiborgia · TaxonDwergenpaartje · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“for I. rautanenii and Wiborgia , nodule isolates B. ripae WR4 T or Mesorhizobium sp. WR52, respectively, were authenticated”

✓ located verbatim in the source · abstract, characters 2248–2371 · show in text ↑