Disentangling the genetic basis of rhizosphere microbiome assembly in tomato

Ben O. Oyserman; Stalin Sarango Flores; Thom Griffioen; Xinya Pan; Elmar van der Wijk; Lotte Pronk; Wouter Lokhorst; Azkia Nurfikari; Joseph N. Paulson; Mercedeh Movassagh; Nejc Stopnisek; Anne Kupczok; Viviane Cordovez; Victor J. Carrion; Wilco Ligterink; Basten L. Snoek; Marnix H. Medema; Jos M. Raaijmakers

doi:10.1038/s41467-022-30849-9

Disentangling the genetic basis of rhizosphere microbiome assembly in tomato

Ben O. Oyserman^* (Corresponding author), Stalin Sarango Flores, Thom Griffioen, Xinya Pan, Elmar van der Wijk, Lotte Pronk, Wouter Lokhorst, Azkia Nurfikari, Joseph N. Paulson, Mercedeh Movassagh, Nejc Stopnisek, Anne Kupczok, Viviane Cordovez, Victor J. Carrion, Wilco Ligterink, Basten L. Snoek, Marnix H. Medema, Jos M. Raaijmakers^* (Corresponding author)

^*Corresponding author for this work

NIOO - Microbial Ecology (ME)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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Abstract

Microbiomes play a pivotal role in plant growth and health, but the genetic factors involved in microbiome assembly remain largely elusive. Here, we map the molecular features of the rhizosphere microbiome as quantitative traits of a diverse hybrid population of wild and domesticated tomato. Gene content analysis of prioritized tomato quantitative trait loci suggests a genetic basis for differential recruitment of various rhizobacterial lineages, including a Streptomyces-associated 6.31 Mbp region harboring tomato domestication sweeps and encoding, among others, the iron regulator FIT and the water channel aquaporin SlTIP2.3. Within metagenome-assembled genomes of root-associated Streptomyces and Cellvibrio, we identify bacterial genes involved in metabolism of plant polysaccharides, iron, sulfur, trehalose, and vitamins, whose genetic variation associates with specific tomato QTLs. By integrating ‘microbiomics’ and quantitative plant genetics, we pinpoint putative plant and reciprocal rhizobacterial traits underlying microbiome assembly, thereby providing a first step towards plant-microbiome breeding programs.

Original language	English
Article number	3228
Number of pages	16
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-30849-9
Publication status	Published - 16 Jun 2022

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7458_OysermanFinal published version, 9.87 MBLicence: CC BY

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Oyserman, B. O., Flores, S. S., Griffioen, T., Pan, X., van der Wijk, E., Pronk, L., Lokhorst, W., Nurfikari, A., Paulson, J. N., Movassagh, M., Stopnisek, N., Kupczok, A., Cordovez, V., Carrion, V. J., Ligterink, W., Snoek, B. L., Medema, M. H., & Raaijmakers, J. M. (2022). Disentangling the genetic basis of rhizosphere microbiome assembly in tomato. Nature Communications, 13(1), Article 3228. https://doi.org/10.1038/s41467-022-30849-9

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abstract = "Microbiomes play a pivotal role in plant growth and health, but the genetic factors involved in microbiome assembly remain largely elusive. Here, we map the molecular features of the rhizosphere microbiome as quantitative traits of a diverse hybrid population of wild and domesticated tomato. Gene content analysis of prioritized tomato quantitative trait loci suggests a genetic basis for differential recruitment of various rhizobacterial lineages, including a Streptomyces-associated 6.31 Mbp region harboring tomato domestication sweeps and encoding, among others, the iron regulator FIT and the water channel aquaporin SlTIP2.3. Within metagenome-assembled genomes of root-associated Streptomyces and Cellvibrio, we identify bacterial genes involved in metabolism of plant polysaccharides, iron, sulfur, trehalose, and vitamins, whose genetic variation associates with specific tomato QTLs. By integrating {\textquoteleft}microbiomics{\textquoteright} and quantitative plant genetics, we pinpoint putative plant and reciprocal rhizobacterial traits underlying microbiome assembly, thereby providing a first step towards plant-microbiome breeding programs.",

author = "Oyserman, {Ben O.} and Flores, {Stalin Sarango} and Thom Griffioen and Xinya Pan and {van der Wijk}, Elmar and Lotte Pronk and Wouter Lokhorst and Azkia Nurfikari and Paulson, {Joseph N.} and Mercedeh Movassagh and Nejc Stopnisek and Anne Kupczok and Viviane Cordovez and Carrion, {Victor J.} and Wilco Ligterink and Snoek, {Basten L.} and Medema, {Marnix H.} and Raaijmakers, {Jos M.}",

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Oyserman, BO, Flores, SS, Griffioen, T, Pan, X, van der Wijk, E, Pronk, L, Lokhorst, W, Nurfikari, A, Paulson, JN, Movassagh, M, Stopnisek, N, Kupczok, A, Cordovez, V, Carrion, VJ, Ligterink, W, Snoek, BL, Medema, MH & Raaijmakers, JM 2022, 'Disentangling the genetic basis of rhizosphere microbiome assembly in tomato', Nature Communications, vol. 13, no. 1, 3228. https://doi.org/10.1038/s41467-022-30849-9

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AU - Flores, Stalin Sarango

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AU - Pan, Xinya

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AU - Pronk, Lotte

AU - Lokhorst, Wouter

AU - Nurfikari, Azkia

AU - Paulson, Joseph N.

AU - Movassagh, Mercedeh

AU - Stopnisek, Nejc

AU - Kupczok, Anne

AU - Cordovez, Viviane

AU - Carrion, Victor J.

AU - Ligterink, Wilco

AU - Snoek, Basten L.

AU - Medema, Marnix H.

AU - Raaijmakers, Jos M.

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AB - Microbiomes play a pivotal role in plant growth and health, but the genetic factors involved in microbiome assembly remain largely elusive. Here, we map the molecular features of the rhizosphere microbiome as quantitative traits of a diverse hybrid population of wild and domesticated tomato. Gene content analysis of prioritized tomato quantitative trait loci suggests a genetic basis for differential recruitment of various rhizobacterial lineages, including a Streptomyces-associated 6.31 Mbp region harboring tomato domestication sweeps and encoding, among others, the iron regulator FIT and the water channel aquaporin SlTIP2.3. Within metagenome-assembled genomes of root-associated Streptomyces and Cellvibrio, we identify bacterial genes involved in metabolism of plant polysaccharides, iron, sulfur, trehalose, and vitamins, whose genetic variation associates with specific tomato QTLs. By integrating ‘microbiomics’ and quantitative plant genetics, we pinpoint putative plant and reciprocal rhizobacterial traits underlying microbiome assembly, thereby providing a first step towards plant-microbiome breeding programs.

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UR - https://www.ebi.ac.uk/ena/browser/view/PRJNA787039

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SN - 2041-1723

VL - 13

JO - Nature Communications

JF - Nature Communications

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ER -

Disentangling the genetic basis of rhizosphere microbiome assembly in tomato

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