The RNAome landscape of tomato during arbuscular mycorrhizal symbiosis reveals an evolving RNA layer symbiotic regulatory network

Zeng, Zhen; Liu, Yang; Feng, Xingyu; Li, Sai-Xi; Jiang, Xing-Mei; Chen, Jian-Qun; Shao, Zhu‐Qing

doi:10.1016/j.xplc.2022.100429

Cited by 18 publications

(18 citation statements)

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“…S4). RNA sequencing data indicate that, compared with nonmycorrhizal roots, the expression of HEXO2 homologs is elevated in mycorrhizal roots in various plants, including tomato (Solyc01g081610; Tominaga et al ., 2022; Zeng et al ., 2023) and rice (LOC_Os07g38790; Fiorilli et al ., 2015; Gutjahr et al ., 2015). The HEXO3 clade appears to lack leguminous genes (Fig.…”

Section: Resultsmentioning

confidence: 99%

An extracellular β‐N‐acetylhexosaminidase of Medicago truncatula hydrolyzes chitooligosaccharides and is involved in arbuscular mycorrhizal symbiosis but not required for nodulation

et al. 2023

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Summary Establishment of symbiosis between plants and arbuscular mycorrhizal (AM) fungi depends on fungal chitooligosaccharides (COs) and lipo‐chitooligosaccharides (LCOs). The latter are also produced by nitrogen‐fixing rhizobia to induce nodules on leguminous roots. However, host enzymes regulating structure and levels of these signals remain largely unknown. Here, we analyzed the expression of a β‐N‐acetylhexosaminidase gene of Medicago truncatula (MtHEXO2) and biochemically characterized the enzyme. Mutant analysis was performed to study the role of MtHEXO2 during symbiosis. We found that expression of MtHEXO2 is associated with AM symbiosis and nodulation. MtHEXO2 expression in the rhizodermis was upregulated in response to applied chitotetraose, chitoheptaose, and LCOs. M. truncatula mutants deficient in symbiotic signaling did not show induction of MtHEXO2. Subcellular localization analysis indicated that MtHEXO2 is an extracellular protein. Biochemical analysis showed that recombinant MtHEXO2 does not cleave LCOs but can degrade COs into N‐acetylglucosamine (GlcNAc). Hexo2 mutants exhibited reduced colonization by AM fungi; however, nodulation was not affected in hexo2 mutants. In conclusion, we identified an enzyme, which inactivates COs and promotes the AM symbiosis. We hypothesize that GlcNAc produced by MtHEXO2 may function as a secondary symbiotic signal.

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Section: Resultsmentioning

confidence: 99%

An extracellular β‐N‐acetylhexosaminidase of Medicago truncatula hydrolyzes chitooligosaccharides and is involved in arbuscular mycorrhizal symbiosis but not required for nodulation

et al. 2023

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“…We also downloaded 75 Illumina RNA-seq datasets and two PacBio RNA-seq datasets involving different tissues/organs and different developmental stages and/or different treatments from our previous study (Zeng et al ., 2022), and a study performed by others (Li et al ., 2020). Twelve microTom tomato proteomic datasets were retrieved from the PRIDE Archive database (Proteomics identifications database, https://www.ebi.ac.uk/pride/archive/).…”

Section: Methodsmentioning

confidence: 99%

“…The microTom tomato has become an emerging model plant system for developmental biology of fruit development (Klee & Giovannoni, 2011; Azzi et al ., 2015), arbuscular mycorrhiza symbiosis (Chitarra et al ., 2016; Liao et al ., 2022) and RNA editing (Yang et al ., 2017; Yang et al ., 2020; Li et al ., 2022) as well, which, however, all focused on organellar RE and the regulators, whereas nuclear RE has not been touched. Therefore in this study, we assembled a high-quality of genome of microTom, together with large amounts of RNA-seq data sequenced in this study and collected from public databases (Li et al ., 2020; Zeng et al ., 2022), we performed comprehensive analyses of RE events in the microTom tomato nuclear genome across different organs/developmental stages/treatments.…”

Section: Introductionmentioning

confidence: 99%

“…With the assistance of three full-length transcriptome and 81 Illumina short read length RNA-seq datasets derived from different organs, under different developmental stages and/or treatments (See Methods and Materials) from this and previous studies (Li et al ., 2020; Zeng et al ., 2022), a total of 35,213 protein-coding genes were annotated ( Figure 1a ), with 31,891 genes (90.57%) receiving transcriptomic data support from at least one RNA-seq sample. The massive RNA-seq data helped to annotate 4,449 “new” genes that were previously “hiding” in the Heinz tomato genome (gene length coverage and DNA sequence identity > 90%), probably due to inadequate RNA-seq data in the Heinz cultivar.…”

Section: Introductionmentioning

confidence: 99%

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Comprehensive regulatory networks for tomato organ development based on the genome and RNAome of microTom tomato

Xue

Fan

Zeng

et al. 2022

Preprint

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Sequence discrepancy between genomic DNA and transcribed RNAs, namely RNA editing (RE), was reported to be extensive in metazoan nuclear genomes and plant organellar genomes, but largely unexplored in plant nuclear genomes. By comparing the tomato microTom RNA-seq data to its newly assembled genome, we, for the first time, detected extensive RE events (37,984 sites in 5,873 genes) on in the plant nuclear genome, which is supported by evidence from both experimental validation and proteomic data. Other than the prevalence of RE in the microTom genome, the biased pattern-transition overwhelmingly outnumbering transversion-rivals that in animals, and may imply an ancient and shared mechanism underlying RE across eukaryotes. We observed conserved RE sites that were always edited under all conditions, and could be considered as "fixed mutations" at the RNA level; also we detected conditional RE sites occurring only in specific organ/developmental stage/treatment, possibly suggesting distinct functional roles. Evolutionarily, RE results in sequence diversity at the RNA level and may lead to even functional innovation of proteins, hence may be considered as an additional mechanism to expand gene diversity other than gene duplications and alternative splicing.

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“…While there is a wealth of literature on the role of sRNAs in plantpathogenic interactions, the current knowledge on the sRNAmediated gene regulation network controlling the AM symbiosis is still limited and possibly represents the tip of the iceberg. The colonization by AM fungi induces an extensive reprogramming of plant sRNAs expression, many of which are conserved in different plant species (Gu et al, 2010;Devers et al, 2011;Formey et al, 2014;Wu et al, 2016;Pandey et al, 2018;Xu et al, 2018;Mewalal et al, 2019;Mendoza-Soto et al, 2022;Zeng et al, 2023;Fig. 1).…”

Section: Plant Srnas Shape Plant-biotic Interactions Including the Am...mentioning

confidence: 99%

A journey into the world of small RNAs in the arbuscular mycorrhizal symbiosis

Ledford,

Silvestri,

Fiorilli

et al. 2023

New Phytologist

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SummaryArbuscular mycorrhizal (AM) symbiosis is a mutualistic interaction between fungi and most land plants that is underpinned by a bidirectional exchange of nutrients. AM development is a tightly regulated process that encompasses molecular communication for reciprocal recognition, fungal accommodation in root tissues and activation of symbiotic function. As such, a complex network of transcriptional regulation and molecular signaling underlies the cellular and metabolic reprogramming of host cells upon AM fungal colonization. In addition to transcription factors, small RNAs (sRNAs) are emerging as important regulators embedded in the gene network that orchestrates AM development. In addition to controlling cell‐autonomous processes, plant sRNAs also function as mobile signals capable of moving to different organs and even to different plants or organisms that interact with plants. AM fungi also produce sRNAs; however, their function in the AM symbiosis remains largely unknown. Here, we discuss the contribution of host sRNAs in the development of AM symbiosis by considering their role in the transcriptional reprogramming of AM fungal colonized cells. We also describe the characteristics of AM fungal‐derived sRNAs and emerging evidence for the bidirectional transfer of functional sRNAs between the two partners to mutually modulate gene expression and control the symbiosis.

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The RNAome landscape of tomato during arbuscular mycorrhizal symbiosis reveals an evolving RNA layer symbiotic regulatory network

Cited by 18 publications

References 123 publications

An extracellular β‐N‐acetylhexosaminidase of Medicago truncatula hydrolyzes chitooligosaccharides and is involved in arbuscular mycorrhizal symbiosis but not required for nodulation

An extracellular β‐N‐acetylhexosaminidase of Medicago truncatula hydrolyzes chitooligosaccharides and is involved in arbuscular mycorrhizal symbiosis but not required for nodulation

Comprehensive regulatory networks for tomato organ development based on the genome and RNAome of microTom tomato

A journey into the world of small RNAs in the arbuscular mycorrhizal symbiosis

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