A rare non-canonical splice site in Trema orientalis SYMRK does not affect its dual symbiotic functioning in endomycorrhiza and rhizobium nodulation

Background: Nitrogen-fixing nodules occur in ten related taxonomic lineages interspersed with lineages of non-nodulating plant species. Nodules result from an endosymbiosis between plants and diazotrophic bacteria; rhizobia in the case of legumes and Parasponia and Frankia in the case of actinorhizal species. Nodulating plants share a conserved set of symbiosis genes, whereas related non-nodulating sister species show pseudogenization of several key nodulation-specific genes. Signalling and cellular mechanisms critical for nodulation have been co-opted from the more ancient plant-fungal arbuscular endomycorrhizal symbiosis. Studies in legumes and actinorhizal plants uncovered a key component in symbiotic signalling, the LRR-type SYMBIOSIS RECEPTOR KINASE (SYMRK). SYMRK is essential for nodulation and arbuscular endomycorrhizal symbiosis. To our surprise, however, despite its arbuscular endomycorrhizal symbiosis capacities, we observed a seemingly critical mutation in a donor splice site in the SYMRK gene of Trema orientalis, the non-nodulating sister species of Parasponia. This led us to investigate the symbiotic functioning of SYMRK in the Trema-Parasponia lineage and to address the question of to what extent a single nucleotide polymorphism in a donor splice site affects the symbiotic functioning of SYMRK. Results: We show that SYMRK is essential for nodulation and endomycorrhization in Parasponia andersonii. Subsequently, it is revealed that the 5’-intron donor splice site of SYMRK intron 12 is variable and, in most dicotyledon species, doesn’t contain the canonical dinucleotide ‘GT’ signature but the much less common motif ‘GC’. Strikingly, in T. orientalis, this motif is converted into a rare non-canonical 5’-intron donor splice site ‘GA’. This SYMRK allele, however, is fully functional and spreads in the T. orientalis population of Malaysian Borneo. A further investigation into the occurrence of the non-canonical GA-AG splice sites confirmed that these are extremely rare. Conclusion: SYMRK functioning is highly conserved in legumes, actinorhizal plants, and Parasponia. The gene possesses a non-common 5’-intron GC donor splice site in intron 12, which is converted into a GA in T. orientalis accessions of Malaysian Borneo. The discovery of this functional GA-AG splice site in SYMRK highlights a gap in our understanding of splice donor sites.

Saved in:
Bibliographic Details
Main Authors: Alhusayni, Sultan, Roswanjaya, Yuda Purwana, Rutten, Luuk, Huisman, Rik, Bertram, S., Sharma, Trupti, Schon, Michael, Kohlen, Wouter, Klein, Joël, Geurts, Rene
Format: Article/Letter to editor biblioteca
Language:English
Subjects:Arbuscular mycorrhizal symbiosis, Common symbiosis signalling pathway, LRR-type transmembrane receptor kinase, Mutualistic endosymbiosis, Nitrogen-fixing nodulation symbiosis, Non-canonical splice site, Parasponia andersonii, Plant evolution, SYMRK, Trema orientalis,
Online Access:https://research.wur.nl/en/publications/a-rare-non-canonical-splice-site-in-trema-orientalis-symrk-does-n
Tags: Add Tag
No Tags, Be the first to tag this record!
id dig-wur-nl-wurpubs-623893
record_format koha
spelling dig-wur-nl-wurpubs-6238932024-10-02 Alhusayni, Sultan Roswanjaya, Yuda Purwana Rutten, Luuk Huisman, Rik Bertram, S. Sharma, Trupti Schon, Michael Kohlen, Wouter Klein, Joël Geurts, Rene Article/Letter to editor BMC Plant Biology 23 (2023) ISSN: 1471-2229 A rare non-canonical splice site in Trema orientalis SYMRK does not affect its dual symbiotic functioning in endomycorrhiza and rhizobium nodulation 2023 Background: Nitrogen-fixing nodules occur in ten related taxonomic lineages interspersed with lineages of non-nodulating plant species. Nodules result from an endosymbiosis between plants and diazotrophic bacteria; rhizobia in the case of legumes and Parasponia and Frankia in the case of actinorhizal species. Nodulating plants share a conserved set of symbiosis genes, whereas related non-nodulating sister species show pseudogenization of several key nodulation-specific genes. Signalling and cellular mechanisms critical for nodulation have been co-opted from the more ancient plant-fungal arbuscular endomycorrhizal symbiosis. Studies in legumes and actinorhizal plants uncovered a key component in symbiotic signalling, the LRR-type SYMBIOSIS RECEPTOR KINASE (SYMRK). SYMRK is essential for nodulation and arbuscular endomycorrhizal symbiosis. To our surprise, however, despite its arbuscular endomycorrhizal symbiosis capacities, we observed a seemingly critical mutation in a donor splice site in the SYMRK gene of Trema orientalis, the non-nodulating sister species of Parasponia. This led us to investigate the symbiotic functioning of SYMRK in the Trema-Parasponia lineage and to address the question of to what extent a single nucleotide polymorphism in a donor splice site affects the symbiotic functioning of SYMRK. Results: We show that SYMRK is essential for nodulation and endomycorrhization in Parasponia andersonii. Subsequently, it is revealed that the 5’-intron donor splice site of SYMRK intron 12 is variable and, in most dicotyledon species, doesn’t contain the canonical dinucleotide ‘GT’ signature but the much less common motif ‘GC’. Strikingly, in T. orientalis, this motif is converted into a rare non-canonical 5’-intron donor splice site ‘GA’. This SYMRK allele, however, is fully functional and spreads in the T. orientalis population of Malaysian Borneo. A further investigation into the occurrence of the non-canonical GA-AG splice sites confirmed that these are extremely rare. Conclusion: SYMRK functioning is highly conserved in legumes, actinorhizal plants, and Parasponia. The gene possesses a non-common 5’-intron GC donor splice site in intron 12, which is converted into a GA in T. orientalis accessions of Malaysian Borneo. The discovery of this functional GA-AG splice site in SYMRK highlights a gap in our understanding of splice donor sites. en application/pdf https://research.wur.nl/en/publications/a-rare-non-canonical-splice-site-in-trema-orientalis-symrk-does-n 10.1186/s12870-023-04594-0 https://edepot.wur.nl/645615 Arbuscular mycorrhizal symbiosis Common symbiosis signalling pathway LRR-type transmembrane receptor kinase Mutualistic endosymbiosis Nitrogen-fixing nodulation symbiosis Non-canonical splice site Parasponia andersonii Plant evolution SYMRK Trema orientalis https://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/ Wageningen University & Research
institution WUR NL
collection DSpace
country Países bajos
countrycode NL
component Bibliográfico
access En linea
databasecode dig-wur-nl
tag biblioteca
region Europa del Oeste
libraryname WUR Library Netherlands
language English
topic Arbuscular mycorrhizal symbiosis
Common symbiosis signalling pathway
LRR-type transmembrane receptor kinase
Mutualistic endosymbiosis
Nitrogen-fixing nodulation symbiosis
Non-canonical splice site
Parasponia andersonii
Plant evolution
SYMRK
Trema orientalis
Arbuscular mycorrhizal symbiosis
Common symbiosis signalling pathway
LRR-type transmembrane receptor kinase
Mutualistic endosymbiosis
Nitrogen-fixing nodulation symbiosis
Non-canonical splice site
Parasponia andersonii
Plant evolution
SYMRK
Trema orientalis
spellingShingle Arbuscular mycorrhizal symbiosis
Common symbiosis signalling pathway
LRR-type transmembrane receptor kinase
Mutualistic endosymbiosis
Nitrogen-fixing nodulation symbiosis
Non-canonical splice site
Parasponia andersonii
Plant evolution
SYMRK
Trema orientalis
Arbuscular mycorrhizal symbiosis
Common symbiosis signalling pathway
LRR-type transmembrane receptor kinase
Mutualistic endosymbiosis
Nitrogen-fixing nodulation symbiosis
Non-canonical splice site
Parasponia andersonii
Plant evolution
SYMRK
Trema orientalis
Alhusayni, Sultan
Roswanjaya, Yuda Purwana
Rutten, Luuk
Huisman, Rik
Bertram, S.
Sharma, Trupti
Schon, Michael
Kohlen, Wouter
Klein, Joël
Geurts, Rene
A rare non-canonical splice site in Trema orientalis SYMRK does not affect its dual symbiotic functioning in endomycorrhiza and rhizobium nodulation
description Background: Nitrogen-fixing nodules occur in ten related taxonomic lineages interspersed with lineages of non-nodulating plant species. Nodules result from an endosymbiosis between plants and diazotrophic bacteria; rhizobia in the case of legumes and Parasponia and Frankia in the case of actinorhizal species. Nodulating plants share a conserved set of symbiosis genes, whereas related non-nodulating sister species show pseudogenization of several key nodulation-specific genes. Signalling and cellular mechanisms critical for nodulation have been co-opted from the more ancient plant-fungal arbuscular endomycorrhizal symbiosis. Studies in legumes and actinorhizal plants uncovered a key component in symbiotic signalling, the LRR-type SYMBIOSIS RECEPTOR KINASE (SYMRK). SYMRK is essential for nodulation and arbuscular endomycorrhizal symbiosis. To our surprise, however, despite its arbuscular endomycorrhizal symbiosis capacities, we observed a seemingly critical mutation in a donor splice site in the SYMRK gene of Trema orientalis, the non-nodulating sister species of Parasponia. This led us to investigate the symbiotic functioning of SYMRK in the Trema-Parasponia lineage and to address the question of to what extent a single nucleotide polymorphism in a donor splice site affects the symbiotic functioning of SYMRK. Results: We show that SYMRK is essential for nodulation and endomycorrhization in Parasponia andersonii. Subsequently, it is revealed that the 5’-intron donor splice site of SYMRK intron 12 is variable and, in most dicotyledon species, doesn’t contain the canonical dinucleotide ‘GT’ signature but the much less common motif ‘GC’. Strikingly, in T. orientalis, this motif is converted into a rare non-canonical 5’-intron donor splice site ‘GA’. This SYMRK allele, however, is fully functional and spreads in the T. orientalis population of Malaysian Borneo. A further investigation into the occurrence of the non-canonical GA-AG splice sites confirmed that these are extremely rare. Conclusion: SYMRK functioning is highly conserved in legumes, actinorhizal plants, and Parasponia. The gene possesses a non-common 5’-intron GC donor splice site in intron 12, which is converted into a GA in T. orientalis accessions of Malaysian Borneo. The discovery of this functional GA-AG splice site in SYMRK highlights a gap in our understanding of splice donor sites.
format Article/Letter to editor
topic_facet Arbuscular mycorrhizal symbiosis
Common symbiosis signalling pathway
LRR-type transmembrane receptor kinase
Mutualistic endosymbiosis
Nitrogen-fixing nodulation symbiosis
Non-canonical splice site
Parasponia andersonii
Plant evolution
SYMRK
Trema orientalis
author Alhusayni, Sultan
Roswanjaya, Yuda Purwana
Rutten, Luuk
Huisman, Rik
Bertram, S.
Sharma, Trupti
Schon, Michael
Kohlen, Wouter
Klein, Joël
Geurts, Rene
author_facet Alhusayni, Sultan
Roswanjaya, Yuda Purwana
Rutten, Luuk
Huisman, Rik
Bertram, S.
Sharma, Trupti
Schon, Michael
Kohlen, Wouter
Klein, Joël
Geurts, Rene
author_sort Alhusayni, Sultan
title A rare non-canonical splice site in Trema orientalis SYMRK does not affect its dual symbiotic functioning in endomycorrhiza and rhizobium nodulation
title_short A rare non-canonical splice site in Trema orientalis SYMRK does not affect its dual symbiotic functioning in endomycorrhiza and rhizobium nodulation
title_full A rare non-canonical splice site in Trema orientalis SYMRK does not affect its dual symbiotic functioning in endomycorrhiza and rhizobium nodulation
title_fullStr A rare non-canonical splice site in Trema orientalis SYMRK does not affect its dual symbiotic functioning in endomycorrhiza and rhizobium nodulation
title_full_unstemmed A rare non-canonical splice site in Trema orientalis SYMRK does not affect its dual symbiotic functioning in endomycorrhiza and rhizobium nodulation
title_sort rare non-canonical splice site in trema orientalis symrk does not affect its dual symbiotic functioning in endomycorrhiza and rhizobium nodulation
url https://research.wur.nl/en/publications/a-rare-non-canonical-splice-site-in-trema-orientalis-symrk-does-n
work_keys_str_mv AT alhusaynisultan ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT roswanjayayudapurwana ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT ruttenluuk ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT huismanrik ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT bertrams ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT sharmatrupti ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT schonmichael ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT kohlenwouter ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT kleinjoel ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT geurtsrene ararenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT alhusaynisultan rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT roswanjayayudapurwana rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT ruttenluuk rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT huismanrik rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT bertrams rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT sharmatrupti rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT schonmichael rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT kohlenwouter rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT kleinjoel rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
AT geurtsrene rarenoncanonicalsplicesiteintremaorientalissymrkdoesnotaffectitsdualsymbioticfunctioninginendomycorrhizaandrhizobiumnodulation
_version_ 1813192519121371136