Heterotypic transcriptional condensates formed by prion-like paralogous proteins canalize flowering transition in tomato
Abstract Background Paralogs that arise from gene duplications during genome evolution enable genetic redundancy and phenotypic robustness. Variation in the coding or regulatory sequence of paralogous transcriptional regulators diversifies their functions and relationships, which provides developmen...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-03-01
|
| Series: | Genome Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13059-022-02646-6 |
| _version_ | 1818773543262879744 |
|---|---|
| author | Xiaozhen Huang Nan Xiao Yupan Zou Yue Xie Lingli Tang Yueqin Zhang Yuan Yu Yiting Li Cao Xu |
| author_facet | Xiaozhen Huang Nan Xiao Yupan Zou Yue Xie Lingli Tang Yueqin Zhang Yuan Yu Yiting Li Cao Xu |
| author_sort | Xiaozhen Huang |
| collection | DOAJ |
| description | Abstract Background Paralogs that arise from gene duplications during genome evolution enable genetic redundancy and phenotypic robustness. Variation in the coding or regulatory sequence of paralogous transcriptional regulators diversifies their functions and relationships, which provides developmental robustness against genetic or environmental perturbation. The fate transition of plant shoot stem cells for flowering and reproductive success requires a robust transcriptional control. However, how paralogs function and interact to achieve such robustness is unknown. Results Here, we explore the genetic relationship and protein behavior of ALOG family transcriptional factors with diverse transcriptional abundance in shoot meristems. A mutant spectrum covers single and higher-order mutant combinations of five ALOG paralogs and creates a continuum of flowering transition defects, showing gradually enhanced precocious flowering, along with inflorescence simplification from wild-type-like to progressively fewer flowers until solitary flower with sterile floral organs. Therefore, these paralogs play unequal roles and act together to achieve a robust genetic canalization. All five proteins contain prion-like intrinsically disordered regions (IDRs) and undergo phase separation. Accumulated mutations following gene duplications lead to IDR variations among ALOG paralogs, resulting in divergent phase separation and transcriptional regulation capabilities. Remarkably, they retain the ancestral abilities to assemble into a heterotypic condensate that prevents precocious activation of the floral identity gene ANANTHA. Conclusions Our study reveals a novel genetic canalization mechanism enabled by heterotypic transcriptional condensates formed by paralogous protein interactions and phase separation, uncovering the molecular link between gene duplication caused IDR variation and robust transcriptional control of stem cell fate transition. |
| first_indexed | 2024-12-18T10:26:55Z |
| format | Article |
| id | doaj.art-6e72b25356fe4ea38fe57fa5bea8029f |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-12-18T10:26:55Z |
| publishDate | 2022-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-6e72b25356fe4ea38fe57fa5bea8029f2022-12-21T21:10:57ZengBMCGenome Biology1474-760X2022-03-0123112110.1186/s13059-022-02646-6Heterotypic transcriptional condensates formed by prion-like paralogous proteins canalize flowering transition in tomatoXiaozhen Huang0Nan Xiao1Yupan Zou2Yue Xie3Lingli Tang4Yueqin Zhang5Yuan Yu6Yiting Li7Cao Xu8State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesState Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesState Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesState Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesState Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesState Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesState Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesState Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesState Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesAbstract Background Paralogs that arise from gene duplications during genome evolution enable genetic redundancy and phenotypic robustness. Variation in the coding or regulatory sequence of paralogous transcriptional regulators diversifies their functions and relationships, which provides developmental robustness against genetic or environmental perturbation. The fate transition of plant shoot stem cells for flowering and reproductive success requires a robust transcriptional control. However, how paralogs function and interact to achieve such robustness is unknown. Results Here, we explore the genetic relationship and protein behavior of ALOG family transcriptional factors with diverse transcriptional abundance in shoot meristems. A mutant spectrum covers single and higher-order mutant combinations of five ALOG paralogs and creates a continuum of flowering transition defects, showing gradually enhanced precocious flowering, along with inflorescence simplification from wild-type-like to progressively fewer flowers until solitary flower with sterile floral organs. Therefore, these paralogs play unequal roles and act together to achieve a robust genetic canalization. All five proteins contain prion-like intrinsically disordered regions (IDRs) and undergo phase separation. Accumulated mutations following gene duplications lead to IDR variations among ALOG paralogs, resulting in divergent phase separation and transcriptional regulation capabilities. Remarkably, they retain the ancestral abilities to assemble into a heterotypic condensate that prevents precocious activation of the floral identity gene ANANTHA. Conclusions Our study reveals a novel genetic canalization mechanism enabled by heterotypic transcriptional condensates formed by paralogous protein interactions and phase separation, uncovering the molecular link between gene duplication caused IDR variation and robust transcriptional control of stem cell fate transition.https://doi.org/10.1186/s13059-022-02646-6ParalogsGene duplicationGenetic redundancyFlowering transitionPhase separationTranscriptional condensates |
| spellingShingle | Xiaozhen Huang Nan Xiao Yupan Zou Yue Xie Lingli Tang Yueqin Zhang Yuan Yu Yiting Li Cao Xu Heterotypic transcriptional condensates formed by prion-like paralogous proteins canalize flowering transition in tomato Genome Biology Paralogs Gene duplication Genetic redundancy Flowering transition Phase separation Transcriptional condensates |
| title | Heterotypic transcriptional condensates formed by prion-like paralogous proteins canalize flowering transition in tomato |
| title_full | Heterotypic transcriptional condensates formed by prion-like paralogous proteins canalize flowering transition in tomato |
| title_fullStr | Heterotypic transcriptional condensates formed by prion-like paralogous proteins canalize flowering transition in tomato |
| title_full_unstemmed | Heterotypic transcriptional condensates formed by prion-like paralogous proteins canalize flowering transition in tomato |
| title_short | Heterotypic transcriptional condensates formed by prion-like paralogous proteins canalize flowering transition in tomato |
| title_sort | heterotypic transcriptional condensates formed by prion like paralogous proteins canalize flowering transition in tomato |
| topic | Paralogs Gene duplication Genetic redundancy Flowering transition Phase separation Transcriptional condensates |
| url | https://doi.org/10.1186/s13059-022-02646-6 |
| work_keys_str_mv | AT xiaozhenhuang heterotypictranscriptionalcondensatesformedbyprionlikeparalogousproteinscanalizefloweringtransitionintomato AT nanxiao heterotypictranscriptionalcondensatesformedbyprionlikeparalogousproteinscanalizefloweringtransitionintomato AT yupanzou heterotypictranscriptionalcondensatesformedbyprionlikeparalogousproteinscanalizefloweringtransitionintomato AT yuexie heterotypictranscriptionalcondensatesformedbyprionlikeparalogousproteinscanalizefloweringtransitionintomato AT linglitang heterotypictranscriptionalcondensatesformedbyprionlikeparalogousproteinscanalizefloweringtransitionintomato AT yueqinzhang heterotypictranscriptionalcondensatesformedbyprionlikeparalogousproteinscanalizefloweringtransitionintomato AT yuanyu heterotypictranscriptionalcondensatesformedbyprionlikeparalogousproteinscanalizefloweringtransitionintomato AT yitingli heterotypictranscriptionalcondensatesformedbyprionlikeparalogousproteinscanalizefloweringtransitionintomato AT caoxu heterotypictranscriptionalcondensatesformedbyprionlikeparalogousproteinscanalizefloweringtransitionintomato |