Genome-wide characterization of the TALE homeodomain family and the KNOX-BLH interaction network in tomato

Key message Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein–protein interaction network of the TALE homeodomain protein family, KNOX and BLH proteins, in tomato leaf and fruit development. KNOTTED-like (KNOX, KN) proteins and BELL1-like (BLH) proteins, which belong to...

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Published inPlant molecular biology Vol. 109; no. 6; pp. 799 - 821
Main Authors Ezura, Kentaro, Nakamura, Akiyoshi, Mitsuda, Nobutaka
Format Journal Article
LanguageEnglish
Published Dordrecht Springer Netherlands 01.08.2022
Springer
Springer Nature B.V
Subjects
Biochemistry
Biomedical and Life Sciences
computer simulation
Dimerization
fruiting
Fruits
Genetic aspects
Genetic research
Genomes
Genomics
Homeobox
homeodomain proteins
KNOX protein
leaf development
Leaves
Life Sciences
molecular biology
Plant Pathology
Plant Sciences
Protein-protein interactions
Proteins
Protoplasts
Sequence analysis
Solanum lycopersicum
Tomatoes
Yeast
yeasts
Expression
Protein–protein interaction
Organ differentiation
KNOX
BLH
Solanum lycopersicum
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Abstract Key message Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein–protein interaction network of the TALE homeodomain protein family, KNOX and BLH proteins, in tomato leaf and fruit development. KNOTTED-like (KNOX, KN) proteins and BELL1-like (BLH) proteins, which belong to the same TALE homeodomain family, act together by forming KNOX-BLH heterodimer modules. These modules play crucial roles in regulating multiple developmental processes in plants, like organ differentiation. However, despite the increasing knowledge about individual KNOX and BLH functions, a comprehensive view of their functional protein–protein interaction (PPI) network remains elusive in most plants, including tomato ( Solanum lycopersicum ), an important model plant to study fruit and leaf development. Here, we characterized eight tomato KNOX genes ( SlKN1 to SlKN8 ) and fourteen tomato BLH genes ( SlBLH1 to SlBLH14 ) by expression profiling, co-expression analysis, and PPI network analysis using two-hybrid techniques in yeasts (Y2H) and protoplasts (P2H). We identified 75 pairwise KNOX-BLH interactions, including ten novel interactors of SlKN2/TKN2, a primary class I KNOX protein, and nine novel interactors of SlKN5, a primary class II KNOX protein. Based on these data, we classified KNOX-BLH modules into several categories, which made us infer the order and combination of the KNOX-BLH modules involved in differentiation processes in leaf and fruit. Notably, the co-expression and interaction of SlKN5 and fruit preferentially expressing BLH1-clade paralogs (SlBLH5/SlBEL11 and SlBLH7) suggest their important roles in regulating fruit differentiation. Furthermore, in silico modeling of the KNOX-BLH modules, sequence analysis, and P2H assay identified several residues and a linker region potentially influencing the affinity of BLHs to KNOXs within their conserved dimerization domains. Together, these findings provide insights into the regulatory mechanism of KNOX-BLH modules underlying tomato organ differentiation.
AbstractList Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein-protein interaction network of the TALE homeodomain protein family, KNOX and BLH proteins, in tomato leaf and fruit development. KNOTTED-like (KNOX, KN) proteins and BELL1-like (BLH) proteins, which belong to the same TALE homeodomain family, act together by forming KNOX-BLH heterodimer modules. These modules play crucial roles in regulating multiple developmental processes in plants, like organ differentiation. However, despite the increasing knowledge about individual KNOX and BLH functions, a comprehensive view of their functional protein-protein interaction (PPI) network remains elusive in most plants, including tomato (Solanum lycopersicum), an important model plant to study fruit and leaf development. Here, we characterized eight tomato KNOX genes (SlKN1 to SlKN8) and fourteen tomato BLH genes (SlBLH1 to SlBLH14) by expression profiling, co-expression analysis, and PPI network analysis using two-hybrid techniques in yeasts (Y2H) and protoplasts (P2H). We identified 75 pairwise KNOX-BLH interactions, including ten novel interactors of SlKN2/TKN2, a primary class I KNOX protein, and nine novel interactors of SlKN5, a primary class II KNOX protein. Based on these data, we classified KNOX-BLH modules into several categories, which made us infer the order and combination of the KNOX-BLH modules involved in differentiation processes in leaf and fruit. Notably, the co-expression and interaction of SlKN5 and fruit preferentially expressing BLH1-clade paralogs (SlBLH5/SlBEL11 and SlBLH7) suggest their important roles in regulating fruit differentiation. Furthermore, in silico modeling of the KNOX-BLH modules, sequence analysis, and P2H assay identified several residues and a linker region potentially influencing the affinity of BLHs to KNOXs within their conserved dimerization domains. Together, these findings provide insights into the regulatory mechanism of KNOX-BLH modules underlying tomato organ differentiation.
Key messageComprehensive yeast and protoplast two-hybrid analyses illustrated the protein–protein interaction network of the TALE homeodomain protein family, KNOX and BLH proteins, in tomato leaf and fruit development.KNOTTED-like (KNOX, KN) proteins and BELL1-like (BLH) proteins, which belong to the same TALE homeodomain family, act together by forming KNOX-BLH heterodimer modules. These modules play crucial roles in regulating multiple developmental processes in plants, like organ differentiation. However, despite the increasing knowledge about individual KNOX and BLH functions, a comprehensive view of their functional protein–protein interaction (PPI) network remains elusive in most plants, including tomato (Solanum lycopersicum), an important model plant to study fruit and leaf development. Here, we characterized eight tomato KNOX genes (SlKN1 to SlKN8) and fourteen tomato BLH genes (SlBLH1 to SlBLH14) by expression profiling, co-expression analysis, and PPI network analysis using two-hybrid techniques in yeasts (Y2H) and protoplasts (P2H). We identified 75 pairwise KNOX-BLH interactions, including ten novel interactors of SlKN2/TKN2, a primary class I KNOX protein, and nine novel interactors of SlKN5, a primary class II KNOX protein. Based on these data, we classified KNOX-BLH modules into several categories, which made us infer the order and combination of the KNOX-BLH modules involved in differentiation processes in leaf and fruit. Notably, the co-expression and interaction of SlKN5 and fruit preferentially expressing BLH1-clade paralogs (SlBLH5/SlBEL11 and SlBLH7) suggest their important roles in regulating fruit differentiation. Furthermore, in silico modeling of the KNOX-BLH modules, sequence analysis, and P2H assay identified several residues and a linker region potentially influencing the affinity of BLHs to KNOXs within their conserved dimerization domains. Together, these findings provide insights into the regulatory mechanism of KNOX-BLH modules underlying tomato organ differentiation.
Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein-protein interaction network of the TALE homeodomain protein family, KNOX and BLH proteins, in tomato leaf and fruit development. KNOTTED-like (KNOX, KN) proteins and BELL1-like (BLH) proteins, which belong to the same TALE homeodomain family, act together by forming KNOX-BLH heterodimer modules. These modules play crucial roles in regulating multiple developmental processes in plants, like organ differentiation. However, despite the increasing knowledge about individual KNOX and BLH functions, a comprehensive view of their functional protein-protein interaction (PPI) network remains elusive in most plants, including tomato (Solanum lycopersicum), an important model plant to study fruit and leaf development. Here, we characterized eight tomato KNOX genes (SlKN1 to SlKN8) and fourteen tomato BLH genes (SlBLH1 to SlBLH14) by expression profiling, co-expression analysis, and PPI network analysis using two-hybrid techniques in yeasts (Y2H) and protoplasts (P2H). We identified 75 pairwise KNOX-BLH interactions, including ten novel interactors of SlKN2/TKN2, a primary class I KNOX protein, and nine novel interactors of SlKN5, a primary class II KNOX protein. Based on these data, we classified KNOX-BLH modules into several categories, which made us infer the order and combination of the KNOX-BLH modules involved in differentiation processes in leaf and fruit. Notably, the co-expression and interaction of SlKN5 and fruit preferentially expressing BLH1-clade paralogs (SlBLH5/SlBEL11 and SlBLH7) suggest their important roles in regulating fruit differentiation. Furthermore, in silico modeling of the KNOX-BLH modules, sequence analysis, and P2H assay identified several residues and a linker region potentially influencing the affinity of BLHs to KNOXs within their conserved dimerization domains. Together, these findings provide insights into the regulatory mechanism of KNOX-BLH modules underlying tomato organ differentiation.KEY MESSAGEComprehensive yeast and protoplast two-hybrid analyses illustrated the protein-protein interaction network of the TALE homeodomain protein family, KNOX and BLH proteins, in tomato leaf and fruit development. KNOTTED-like (KNOX, KN) proteins and BELL1-like (BLH) proteins, which belong to the same TALE homeodomain family, act together by forming KNOX-BLH heterodimer modules. These modules play crucial roles in regulating multiple developmental processes in plants, like organ differentiation. However, despite the increasing knowledge about individual KNOX and BLH functions, a comprehensive view of their functional protein-protein interaction (PPI) network remains elusive in most plants, including tomato (Solanum lycopersicum), an important model plant to study fruit and leaf development. Here, we characterized eight tomato KNOX genes (SlKN1 to SlKN8) and fourteen tomato BLH genes (SlBLH1 to SlBLH14) by expression profiling, co-expression analysis, and PPI network analysis using two-hybrid techniques in yeasts (Y2H) and protoplasts (P2H). We identified 75 pairwise KNOX-BLH interactions, including ten novel interactors of SlKN2/TKN2, a primary class I KNOX protein, and nine novel interactors of SlKN5, a primary class II KNOX protein. Based on these data, we classified KNOX-BLH modules into several categories, which made us infer the order and combination of the KNOX-BLH modules involved in differentiation processes in leaf and fruit. Notably, the co-expression and interaction of SlKN5 and fruit preferentially expressing BLH1-clade paralogs (SlBLH5/SlBEL11 and SlBLH7) suggest their important roles in regulating fruit differentiation. Furthermore, in silico modeling of the KNOX-BLH modules, sequence analysis, and P2H assay identified several residues and a linker region potentially influencing the affinity of BLHs to KNOXs within their conserved dimerization domains. Together, these findings provide insights into the regulatory mechanism of KNOX-BLH modules underlying tomato organ differentiation.
KEY MESSAGE: Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein–protein interaction network of the TALE homeodomain protein family, KNOX and BLH proteins, in tomato leaf and fruit development. KNOTTED-like (KNOX, KN) proteins and BELL1-like (BLH) proteins, which belong to the same TALE homeodomain family, act together by forming KNOX-BLH heterodimer modules. These modules play crucial roles in regulating multiple developmental processes in plants, like organ differentiation. However, despite the increasing knowledge about individual KNOX and BLH functions, a comprehensive view of their functional protein–protein interaction (PPI) network remains elusive in most plants, including tomato (Solanum lycopersicum), an important model plant to study fruit and leaf development. Here, we characterized eight tomato KNOX genes (SlKN1 to SlKN8) and fourteen tomato BLH genes (SlBLH1 to SlBLH14) by expression profiling, co-expression analysis, and PPI network analysis using two-hybrid techniques in yeasts (Y2H) and protoplasts (P2H). We identified 75 pairwise KNOX-BLH interactions, including ten novel interactors of SlKN2/TKN2, a primary class I KNOX protein, and nine novel interactors of SlKN5, a primary class II KNOX protein. Based on these data, we classified KNOX-BLH modules into several categories, which made us infer the order and combination of the KNOX-BLH modules involved in differentiation processes in leaf and fruit. Notably, the co-expression and interaction of SlKN5 and fruit preferentially expressing BLH1-clade paralogs (SlBLH5/SlBEL11 and SlBLH7) suggest their important roles in regulating fruit differentiation. Furthermore, in silico modeling of the KNOX-BLH modules, sequence analysis, and P2H assay identified several residues and a linker region potentially influencing the affinity of BLHs to KNOXs within their conserved dimerization domains. Together, these findings provide insights into the regulatory mechanism of KNOX-BLH modules underlying tomato organ differentiation.
Key message Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein–protein interaction network of the TALE homeodomain protein family, KNOX and BLH proteins, in tomato leaf and fruit development. KNOTTED-like (KNOX, KN) proteins and BELL1-like (BLH) proteins, which belong to the same TALE homeodomain family, act together by forming KNOX-BLH heterodimer modules. These modules play crucial roles in regulating multiple developmental processes in plants, like organ differentiation. However, despite the increasing knowledge about individual KNOX and BLH functions, a comprehensive view of their functional protein–protein interaction (PPI) network remains elusive in most plants, including tomato ( Solanum lycopersicum ), an important model plant to study fruit and leaf development. Here, we characterized eight tomato KNOX genes ( SlKN1 to SlKN8 ) and fourteen tomato BLH genes ( SlBLH1 to SlBLH14 ) by expression profiling, co-expression analysis, and PPI network analysis using two-hybrid techniques in yeasts (Y2H) and protoplasts (P2H). We identified 75 pairwise KNOX-BLH interactions, including ten novel interactors of SlKN2/TKN2, a primary class I KNOX protein, and nine novel interactors of SlKN5, a primary class II KNOX protein. Based on these data, we classified KNOX-BLH modules into several categories, which made us infer the order and combination of the KNOX-BLH modules involved in differentiation processes in leaf and fruit. Notably, the co-expression and interaction of SlKN5 and fruit preferentially expressing BLH1-clade paralogs (SlBLH5/SlBEL11 and SlBLH7) suggest their important roles in regulating fruit differentiation. Furthermore, in silico modeling of the KNOX-BLH modules, sequence analysis, and P2H assay identified several residues and a linker region potentially influencing the affinity of BLHs to KNOXs within their conserved dimerization domains. Together, these findings provide insights into the regulatory mechanism of KNOX-BLH modules underlying tomato organ differentiation.
Audience Academic
Author Mitsuda, Nobutaka
Ezura, Kentaro
Nakamura, Akiyoshi
Author_xml – sequence: 1
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  surname: Ezura
  fullname: Ezura, Kentaro
  email: ezura-k@aist.go.jp, agariiri@gmail.com
  organization: Japan Society for the Promotion of Science, Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology
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  givenname: Akiyoshi
  surname: Nakamura
  fullname: Nakamura, Akiyoshi
  organization: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology
– sequence: 3
  givenname: Nobutaka
  surname: Mitsuda
  fullname: Mitsuda, Nobutaka
  organization: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35543849$$D View this record in MEDLINE/PubMed
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ID FETCH-LOGICAL-c513t-693bf3d42264318dcb339633241cf9cce22d23207c398b8f58764d157e1283523
IEDL.DBID U2A
ISSN 0167-4412
1573-5028
IngestDate Fri Jul 11 08:53:50 EDT 2025
Mon Jul 21 11:57:48 EDT 2025
Fri Jul 25 10:22:15 EDT 2025
Tue Jun 10 21:04:12 EDT 2025
Wed Feb 19 02:25:41 EST 2025
Tue Jul 01 00:25:30 EDT 2025
Thu Apr 24 22:57:23 EDT 2025
Fri Feb 21 02:45:17 EST 2025
IsPeerReviewed true
IsScholarly true
Issue 6
Keywords Expression
Protein–protein interaction
Organ differentiation
KNOX
BLH
Solanum lycopersicum
Language English
License 2022. The Author(s), under exclusive licence to Springer Nature B.V.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c513t-693bf3d42264318dcb339633241cf9cce22d23207c398b8f58764d157e1283523
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  year: 2022
  text: 2022-08-01
  day: 01
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PublicationSubtitle An International Journal on Molecular Biology, Molecular Genetics and Biochemistry
PublicationTitle Plant molecular biology
PublicationTitleAbbrev Plant Mol Biol
PublicationTitleAlternate Plant Mol Biol
PublicationYear 2022
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Snippet Key message Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein–protein interaction network of the TALE homeodomain protein family,...
Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein-protein interaction network of the TALE homeodomain protein family, KNOX and BLH...
Key message Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein-protein interaction network of the TALE homeodomain protein family,...
Key messageComprehensive yeast and protoplast two-hybrid analyses illustrated the protein–protein interaction network of the TALE homeodomain protein family,...
KEY MESSAGE: Comprehensive yeast and protoplast two-hybrid analyses illustrated the protein–protein interaction network of the TALE homeodomain protein family,...
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SubjectTerms Biochemistry
Biomedical and Life Sciences
computer simulation
Dimerization
fruiting
Fruits
Genetic aspects
Genetic research
Genomes
Genomics
Homeobox
homeodomain proteins
KNOX protein
leaf development
Leaves
Life Sciences
molecular biology
Plant Pathology
Plant Sciences
Protein-protein interactions
Proteins
Protoplasts
Sequence analysis
Solanum lycopersicum
Tomatoes
Yeast
yeasts
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Title Genome-wide characterization of the TALE homeodomain family and the KNOX-BLH interaction network in tomato
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