Root cap is an important determinant of rhizosphere microbiome assembly

Rüger, Lioba; Ganther, Minh; Freudenthal, Jule; Jansa, Jan; Heintz‐Buschart, Anna; Tarkka, Mika; Bonkowski, Michael

doi:10.1111/nph.19002

Cited by 18 publications

(10 citation statements)

References 156 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The underlying mechanisms currently include (i) competition for niche space, which directly determined whether the beneficial rhizosphere microbiome successful colonization on the root surface [ 9 , 14 , 25 ],(ii) inhibition from secondary metabolites, which determined metabolite exchange networks between rhizosphere microbiome and plant roots via potential allelopathy effect [ 41 , 58 ],(iii) regulation of gene expression in plants, which would affected plant hormone signal transduction and immune system activities (tolerance or avoidance) via the process of microbial inheritance in plants [ 1 , 38 ]. Furthermore, pioneer studies indicated that root hairs are able to influence the rhizosphere microbiome assemblage, and in turn rhizosphere microbes are able to interact with plant-modifying root hairs [ 34 , 55 ]. Root hairs have physical properties that play vital roles in the two-way interaction by specifically changing the plant–microbe interaction interface [ 44 ].…”

Section: Discussionmentioning

confidence: 99%

Host genotype-specific rhizosphere fungus enhances drought resistance in wheat

Yue,

Sun,

Wang

et al. 2024

Microbiome

View full text Add to dashboard Cite

Background The severity and frequency of drought are expected to increase substantially in the coming century and dramatically reduce crop yields. Manipulation of rhizosphere microbiomes is an emerging strategy for mitigating drought stress in agroecosystems. However, little is known about the mechanisms underlying how drought-resistant plant recruitment of specific rhizosphere fungi enhances drought adaptation of drought-sensitive wheats. Here, we investigated microbial community assembly features and functional profiles of rhizosphere microbiomes related to drought-resistant and drought-sensitive wheats by amplicon and shotgun metagenome sequencing techniques. We then established evident linkages between root morphology traits and putative keystone taxa based on microbial inoculation experiments. Furthermore, root RNA sequencing and RT-qPCR were employed to explore the mechanisms how rhizosphere microbes modify plant response traits to drought stresses. Results Our results indicated that host plant signature, plant niche compartment, and planting site jointly contribute to the variation of soil microbiome assembly and functional adaptation, with a relatively greater effect of host plant signature observed for the rhizosphere fungi community. Importantly, drought-resistant wheat (Yunhan 618) possessed more diverse bacterial and fungal taxa than that of the drought-sensitive wheat (Chinese Spring), particularly for specific fungal species. In terms of microbial interkingdom association networks, the drought-resistant variety possessed more complex microbial networks. Metagenomics analyses further suggested that the enriched rhizosphere microbiomes belonging to the drought-resistant cultivar had a higher investment in energy metabolism, particularly in carbon cycling, that shaped their distinctive drought tolerance via the mediation of drought-induced feedback functional pathways. Furthermore, we observed that host plant signature drives the differentiation in the ecological role of the cultivable fungal species Mortierella alpine (M. alpina) and Epicoccum nigrum (E. nigrum). The successful colonization of M. alpina on the root surface enhanced the resistance of wheats in response to drought stresses via activation of drought-responsive genes (e.g., CIPK9 and PP2C30). Notably, we found that lateral roots and root hairs were significantly suppressed by co-colonization of a drought-enriched fungus (M. alpina) and a drought-depleted fungus (E. nigrum). Conclusions Collectively, our findings revealed host genotypes profoundly influence rhizosphere microbiome assembly and functional adaptation, as well as it provides evidence that drought-resistant plant recruitment of specific rhizosphere fungi enhances drought tolerance of drought-sensitive wheats. These findings significantly underpin our understanding of the complex feedbacks between plants and microbes during drought, and lay a foundation for steering “beneficial keystone biome” to develop more resilient and productive crops under climate change.

show abstract

Section: Discussionmentioning

confidence: 99%

Host genotype-specific rhizosphere fungus enhances drought resistance in wheat

Yue,

Sun,

Wang

et al. 2024

Microbiome

View full text Add to dashboard Cite

show abstract

“…For comparison, we also imaged the root cap, which has been shown to be the first point of contact for bacterial cells attempting to colonize the root 36 . Additionally, the root cap may act as a filter that prevents further microbial colonization in the root 37 .…”

Section: Resultsmentioning

confidence: 99%

Label-free functional analysis of root-associated microbes with dynamic quantitative oblique back-illumination microscopy

Filan,

Green,

Diering

et al. 2024

Sci Rep

View full text Add to dashboard Cite

The increasing global demand for food, coupled with concerns about the environmental impact of synthetic fertilizers, underscores the urgency of developing sustainable agricultural practices. Nitrogen-fixing bacteria, known as diazotrophs, offer a potential solution by converting atmospheric nitrogen into bioavailable forms, reducing the reliance on synthetic fertilizers. However, a deeper understanding of their interactions with plants and other microbes is needed. In this study, we introduce a recently developed label-free 3D quantitative phase imaging technology called dynamic quantitative oblique back-illumination microscopy (DqOBM) to assess the functional dynamic activity of diazotrophs in vitro and in situ. Our experiments involved three different diazotrophs (Sinorhizobium meliloti, Azotobacter vinelandii, and Rahnella aquatilis) cultured on media with amendments of carbon and nitrogen sources. Over 5 days, we observed increased dynamics in nutrient-amended media. These results suggest that the observed bacterial dynamics correlate with their metabolic activity. Furthermore, we applied qOBM to visualize microbial dynamics within the root cap and elongation zone of Arabidopsis thaliana primary roots. This allowed us to identify distinct areas of microbial infiltration in plant roots without the need for fluorescent markers. Our findings demonstrate that DqOBM can effectively characterize microbial dynamics and provide insights into plant-microbe interactions in situ, offering a valuable tool for advancing our understanding of sustainable agriculture.

show abstract

“…Likewise, malfunctions within regulated cell death in mammal gut epithelial cells produce death-induced nutrient release (DINNR) that can fuel bacterial growth and infection and could cause a variety of disorders such as inflammatory diseases 34 . The importance of an intact root cap in plant-microbe interactions is further highlighter by the fact that the physical removal of root caps in maize plants leads to increased colonization of the root tip by the plant growth promoting rhizobacterium (PGPR) Pseudomonas fluorescens 35 and to changes in the rhizosphere microbiome composition along the root axis 36 . Moreover, it has been suggested that border cells released from the root cap may distract root-feeding nematodes from attacking plant roots 37 .…”

Section: Discussionmentioning

confidence: 99%

Root cap cell corpse clearance limits microbial colonization inArabidopsis thaliana

Charura

Llamas

Quattro

et al. 2023

Preprint

View full text Add to dashboard Cite

In plants, programmed cell death (PCD) is a fundamental cellular process during development that can also be triggered upon biotic and abiotic stresses. In Arabidopsis thaliana, PCD is an integral part of the differentiation process of the root cap, a specialized organ that surrounds the meristematic stem cells. The acquisition of cell death competence in lateral root cap (LRC) cells depends on the root cap-specific transcription factor ANAC033/SOMBRERO (SMB). Cell death is followed by a rapid cell-autonomous corpse clearing process on the root surface involving the senescence-associated nuclease BFN1 downstream of SMB. Based on transcriptomic datasets we observed the downregulation of BFN1 during Serendipita indica colonization in Arabidopsis, which prompted us to investigate the roles of SMB and BFN1 in fungal accommodation. We show that roots of smb3 mutants, which are deficient in root cap PCD and corpse clearance, are entirely covered by undegraded LRC cell corpses loaded with protein aggregates. The accumulation of uncleared cell corpses promotes intra- and extraradical colonization by S. indica, which in turn is sufficient to subsequently clear the cell corpses from the surface of smb3 roots. Compared to smb3, the bfn1-1 knockout mutant exhibits an attenuated corpse clearance phenotype, but still enhances colonization by S. indica. These results highlight the importance of root cap differentiation in plant-microbe interactions and show that the constant production and clearance of LRC cells represents a sophisticated physical defense mechanism to prevent microbial colonization in close proximity to meristematic stem cells. Furthermore, we propose a mechanism by which S. indica manipulates developmental PCD in Arabidopsis roots by downregulating BFN1 to promote fungal colonization through reduced clearance of dead LRC cells as a potential source of nutrients.

show abstract

Root cap is an important determinant of rhizosphere microbiome assembly

Cited by 18 publications

References 156 publications

Host genotype-specific rhizosphere fungus enhances drought resistance in wheat

Host genotype-specific rhizosphere fungus enhances drought resistance in wheat

Label-free functional analysis of root-associated microbes with dynamic quantitative oblique back-illumination microscopy

Root cap cell corpse clearance limits microbial colonization inArabidopsis thaliana

Contact Info

Product

Resources

About