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Cited by 3Plant Molecular Biology ResearchPlant Parasitism and ResistanceLight effects on plants

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Canonical and Alternative Auxin Signaling Systems in Mono-, Di-, and Tetraploid Potatoes

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Lomin, Sergey N., Kolachevskaya, Oksana O., Arkhipov, Dmitry V., Romanov, Georgy A.·2023·International Journal of Molecular Sciences
DOI 10.3390/ijms241411408PMC PMC10380454

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Abstract

It has long been known that the phytohormone auxin plays a promoting role in tuber formation and stress tolerance in potatoes. Our study aimed to identify and characterize the complete sets of auxin-related genes that presumably constitute the entire auxin signaling system in potato (Solanum tuberosum L.). The corresponding genes were retrieved from sequenced genomes of the doubled monoploid S. tuberosum DM1-3-516-R44 (DM) of the Phureja group, the heterozygous diploid line RH89-039-16 (RH), and the autotetraploid cultivar Otava. Both canonical and noncanonical auxin signaling pathways were considered. Phylogenetic and domain analyses of deduced proteins were supplemented by expression profiling and 3D molecular modeling. The canonical and ABP1-mediated pathways of auxin signaling appeared to be well conserved. The total number of potato genes/proteins presumably involved in canonical auxin signaling is 46 and 108 in monoploid DM and tetraploid Otava, respectively. Among the studied potatoes, spectra of expressed genes obviously associated with auxin signaling were partly cultivar-specific and quite different from analogous spectrum in Arabidopsis. Most of the noncanonical pathways found in Arabidopsis appeared to have low probability in potato. This was equally true for all cultivars used irrespective of their ploidy. Thus, some important features of the (noncanonical) auxin signaling pathways may be variable and species-specific.

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Figures

Figure 1 Overall structures and typical domain composition of auxin signaling-related proteins of potatoes. 1—StTIR1s, StAFBs—presumable auxin receptors. 2—StARF5, 6a, 6b, 8a, 8b, 8c, 19a, 19b, 19c—presumable transcription stimulators; StARF4; StARF1, 2a, 2b, 18a, 18b, 18c—presumable transcription inhibitors. 3—StARF3/ETT, putative noncanonical auxin receptors. 4—StAux/IAA1–4, 6–8, 10–12, 14, 15, 21–23, 25—presumable signal transduction inhibitors. 5—putative noncanonical StAux/IAAs. 6—StTPL, StTPRs—presumable transcription inhibitors. 7—StSKP2A/B—S-Phase Kinase-Associated Protein 2 homolog. 8—StABP1—presumable alternative auxin receptor. 9—StTMK1a, 1b, 4a, 4b, 4c, 5a, 5b, 5c—putative Ser/Thr protein kinases. 10—StTMK1c—TMK-lacking kinase domain. 11—StMPK1, 2—presumable MAP kinases.
Figure 1 Overall structures and typical domain composition of auxin signaling-related proteins of potatoes. 1—StTIR1s, StAFBs—presumable auxin receptors. 2—StARF5, 6a, 6b, 8a, 8b, 8c, 19a, 19b, 19c—presumable transcription stimulators; StARF4; StARF1, 2a, 2b, 18a, 18b, 18c—presumable transcription inhibitors. 3—StARF3/ETT, putative noncanonical auxin receptors. 4—StAux/IAA1–4, 6–8, 10–12, 14, 15, 21–23, 25—presumable signal transduction inhibitors. 5—putative noncanonical StAux/IAAs. 6—StTPL, StTPRs—presumable transcription inhibitors. 7—StSKP2A/B—S-Phase Kinase-Associated Protein 2 homolog. 8—StABP1—presumable alternative auxin receptor. 9—StTMK1a, 1b, 4a, 4b, 4c, 5a, 5b, 5c—putative Ser/Thr protein kinases. 10—StTMK1c—TMK-lacking kinase domain. 11—StMPK1, 2—presumable MAP kinases.CC BY · PubMed Central
Figure 2 Phylogenetic analysis of TIR1/AFB auxin receptor orthologs. The protein sequences of potato, tomato, Arabidopsis, and rice were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. The percentage of replicate trees in which the associated proteins clustered together in the bootstrap test (1000 replicates) are shown next to the branches. The evolutionary distances were computed using the p-distance method. Gene classes are indicated with different colors.
Figure 2 Phylogenetic analysis of TIR1/AFB auxin receptor orthologs. The protein sequences of potato, tomato, Arabidopsis, and rice were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. The percentage of replicate trees in which the associated proteins clustered together in the bootstrap test (1000 replicates) are shown next to the branches. The evolutionary distances were computed using the p-distance method. Gene classes are indicated with different colors.CC BY · PubMed Central
Figure 3 Phylogenetic analysis of ARF transcription regulator orthologs. The protein sequences of potato and Arabidopsis were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. For details, see legend to Figure 2 and Section 3.
Figure 3 Phylogenetic analysis of ARF transcription regulator orthologs. The protein sequences of potato and Arabidopsis were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. For details, see legend to Figure 2 and Section 3.CC BY · PubMed Central
Figure 4 Phylogenetic analysis of Aux/IAA repressors of auxin signaling. The protein sequences of potato and Arabidopsis were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. The evolutionary distances were computed using the equal input method. For details, see legend to Figure 2 and Section 3.
Figure 4 Phylogenetic analysis of Aux/IAA repressors of auxin signaling. The protein sequences of potato and Arabidopsis were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. The evolutionary distances were computed using the equal input method. For details, see legend to Figure 2 and Section 3.CC BY · PubMed Central
Figure 5 Phylogenetic analysis of TPL/TPR chromatin repressors. The protein sequences of potato, tomato, rice, and Arabidopsis were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. For details, see legend to Figure 2 and Section 3.
Figure 5 Phylogenetic analysis of TPL/TPR chromatin repressors. The protein sequences of potato, tomato, rice, and Arabidopsis were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. For details, see legend to Figure 2 and Section 3.CC BY · PubMed Central
Figure 6 Phylogenetic analysis of proteins presumably involved in noncanonical auxin signaling. The protein sequences of potato, tomato, rice, and Arabidopsis were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. For details, see legend to Figure 2 and Section 3. (a). TMK1-like protein kinases. (b). SKP2 F-box proteins. (c). MPK protein kinases.
Figure 6 Phylogenetic analysis of proteins presumably involved in noncanonical auxin signaling. The protein sequences of potato, tomato, rice, and Arabidopsis were retrieved from NCBI database, and phylogenetic analysis was performed with MEGA6 program using neighbor-joining method. For details, see legend to Figure 2 and Section 3. (a). TMK1-like protein kinases. (b). SKP2 F-box proteins. (c). MPK protein kinases.CC BY · PubMed Central
Figure 7 Organ-specific transcriptome profiling in potato cultivars of different ploidy. Upper panel: left, DM potato; right, RH potato. Lower panel: comparison of gene expression patterns in potato cv. Désirée.
Figure 7 Organ-specific transcriptome profiling in potato cultivars of different ploidy. Upper panel: left, DM potato; right, RH potato. Lower panel: comparison of gene expression patterns in potato cv. Désirée.CC BY · PubMed Central
Figure 8 Modeling of 3D structure of canonical auxin receptors of TIR1 family: (a) Model of the spatial structure of canonical potato receptor StTIR1a in complex with IAA and IP6 ligands, StSKP1b protein (marked grey), and a peptide fragment of StAux/IAA23 protein. The F-box site of TIR1 receptor is stained yellow, the LRR domain is stained blue. Transport inhibitor response 1 motif (TIR1/Transp_inhibit) is highlighted in green; C-terminal cap is marked in cyan; adenylate cyclase (AC) motif is marked in magenta. In the ligands, oxygen atoms are colored red, nitrogen atoms are blue, phosphorus atoms are orange, carbon atoms are colored yellow in IAA and gray in IP6. (b) IAA- and IP6-binding sites in StTIR1a are highlighted in the left circle; the right circle shows the IAA binding diagram obtained in LigPlot. (c) Molecular model of potato SCF complex, obtained using AlphaFold multimer. StTIR1a (LRR domain)—blue; StTIR1a (F-box domain)—yellow; StSKP1b—grey; StCUL1—pink; StRBX1—red. (d) Models of the spatial structure of canonical potato TIR1 family auxin receptors (in complex with same ligands and proteins as StTIR1a), compared with the crystal structure of the Arabidopsis AtTIR1 receptor complex with the same ligands, the AtSKP1a protein (marked grey), and the peptide fragment of the AtAux/IAA7 protein (PDB ID: 2P1Q) [66]. Color scheme is the same as in (a) block; lower circles show the IAA binding diagrams obtained in LigPlot. (e) Homology model of the StTIR1a receptor (in three projections) in complex with IAA and IP6. Illustrated representation (top): blue color indicates the LRR domain, yellow indicates the F-box domain. Electrostatic potential of the molecular surface (bottom). Red—negative charge, blue—positive charge, white—neutral zones.
Figure 8 Modeling of 3D structure of canonical auxin receptors of TIR1 family: (a) Model of the spatial structure of canonical potato receptor StTIR1a in complex with IAA and IP6 ligands, StSKP1b protein (marked grey), and a peptide fragment of StAux/IAA23 protein. The F-box site of TIR1 receptor is stained yellow, the LRR domain is stained blue. Transport inhibitor response 1 motif (TIR1/Transp_inhibit) is highlighted in green; C-terminal cap is marked in cyan; adenylate cyclase (AC) motif is marked in magenta. In the ligands, oxygen atoms are colored red, nitrogen atoms are blue, phosphorus atoms are orange, carbon atoms are colored yellow in IAA and gray in IP6. (b) IAA- and IP6-binding sites in StTIR1a are highlighted in the left circle; the right circle shows the IAA binding diagram obtained in LigPlot. (c) Molecular model of potato SCF complex, obtained using AlphaFold multimer. StTIR1a (LRR domain)—blue; StTIR1a (F-box domain)—yellow; StSKP1b—grey; StCUL1—pink; StRBX1—red. (d) Models of the spatial structure of canonical potato TIR1 family auxin receptors (in complex with same ligands and proteins as StTIR1a), compared with the crystal structure of the Arabidopsis AtTIR1 receptor complex with the same ligands, the AtSKP1a protein (marked grey), and the peptide fragment of the AtAux/IAA7 protein (PDB ID: 2P1Q) [66]. Color scheme is the same as in (a) block; lower circles show the IAA binding diagrams obtained in LigPlot. (e) Homology model of the StTIR1a receptor (in three projections) in complex with IAA and IP6. Illustrated representation (top): blue color indicates the LRR domain, yellow indicates the F-box domain. Electrostatic potential of the molecular surface (bottom). Red—negative charge, blue—positive charge, white—neutral zones.CC BY · PubMed Central
Figure 9 The 3D structure of the auxin-binding proteins of the ABP1 family. Comparison of the ABP homology model of potato StABP1 (green) with the crystal structure of maize ZmABP1 (pink) (PDB ID: 1LRH) [79]. Top, full-length ABP dimers. Bottom, ligand-binding patterns: NAA to ZmABP1 (left) in the crystal structure; NAA to StABP1 (center) in the homology model; and docking of IAA to the StABP1 model (right). Red arcs indicate residues that form hydrophobic contacts with the ligand, according to the LigPlot analysis. The blue sphere is the Zn2+ ion.
Figure 9 The 3D structure of the auxin-binding proteins of the ABP1 family. Comparison of the ABP homology model of potato StABP1 (green) with the crystal structure of maize ZmABP1 (pink) (PDB ID: 1LRH) [79]. Top, full-length ABP dimers. Bottom, ligand-binding patterns: NAA to ZmABP1 (left) in the crystal structure; NAA to StABP1 (center) in the homology model; and docking of IAA to the StABP1 model (right). Red arcs indicate residues that form hydrophobic contacts with the ligand, according to the LigPlot analysis. The blue sphere is the Zn2+ ion.CC BY · PubMed Central
Figure 10 Comparison of models of the canonical receptor StTIR1a with a potential protein involved in noncanonical signaling, StSKP2A/B. Noteworthy is the absence of the LRR domain fragment (blue) in StSKP2A/B, which is involved in auxin binding. The colors of the ligand atoms are similar to those in Figure 8. The F-box domain is marked yellow.
Figure 10 Comparison of models of the canonical receptor StTIR1a with a potential protein involved in noncanonical signaling, StSKP2A/B. Noteworthy is the absence of the LRR domain fragment (blue) in StSKP2A/B, which is involved in auxin binding. The colors of the ligand atoms are similar to those in Figure 8. The F-box domain is marked yellow.CC BY · PubMed Central
Figure 11 Spatial structure of canonical ARF auxin signaling transcription factors. Top—structures of the dimer DBD domains in complex with the promoter-like DNA sequence; DBD subdomains are highlighted in color: B3 DBD is green, DD is blue, and AD is red. Bottom shows dimers of PB1 (III/IV) domains. Potato StARF4 (right) and StARF5 (left) protein homology models are compared with the crystal structures (center) of the DBD domain of AtARF1 (PDB ID: 4LDX) [80] and the PB1 domain of AtARF5 (PDB ID: 4CHK) [81] of A. thaliana.
Figure 11 Spatial structure of canonical ARF auxin signaling transcription factors. Top—structures of the dimer DBD domains in complex with the promoter-like DNA sequence; DBD subdomains are highlighted in color: B3 DBD is green, DD is blue, and AD is red. Bottom shows dimers of PB1 (III/IV) domains. Potato StARF4 (right) and StARF5 (left) protein homology models are compared with the crystal structures (center) of the DBD domain of AtARF1 (PDB ID: 4LDX) [80] and the PB1 domain of AtARF5 (PDB ID: 4CHK) [81] of A. thaliana.CC BY · PubMed Central
Figure 12 Molecular models of StTPL (a,b), StTMK1a (c–e), and StMPK1 (e) functional domains. (a) De novo model of StTPL TOPLESS domain (TPD). (b) De novo model of the upstream (N-terminal) WD40 domain of StTPL. (c) Homology model of StTMK1a LRR domains. (d) Homology model of StTMK1a Tyr and Ser/Thr protein kinase domain in complex with ATP molecule and Mg2+ ion. (e) Comparison of StMPK1 and StTMK1a protein kinase domains’ molecular models and their active sites. Homology model of StMPK1 protein kinase domain constructed in complex with phosphoaminophosphonic acid-adenylate ester (ANP) molecule and Mg2+ ion. Active sites are highlighted and magnified. The circles on the right show schemes of interactions with ligands obtained in the LigPlot program. StMPK1 stained yellow, StTMK1a sandy brown. In the ligands, oxygen atoms are colored red, nitrogen atoms are blue, phosphorus atoms are orange, carbon atoms are colored light blue in ANP and aquamarine in ATP. Mg2+ ions are represented as green spheres.
Figure 12 Molecular models of StTPL (a,b), StTMK1a (c–e), and StMPK1 (e) functional domains. (a) De novo model of StTPL TOPLESS domain (TPD). (b) De novo model of the upstream (N-terminal) WD40 domain of StTPL. (c) Homology model of StTMK1a LRR domains. (d) Homology model of StTMK1a Tyr and Ser/Thr protein kinase domain in complex with ATP molecule and Mg2+ ion. (e) Comparison of StMPK1 and StTMK1a protein kinase domains’ molecular models and their active sites. Homology model of StMPK1 protein kinase domain constructed in complex with phosphoaminophosphonic acid-adenylate ester (ANP) molecule and Mg2+ ion. Active sites are highlighted and magnified. The circles on the right show schemes of interactions with ligands obtained in the LigPlot program. StMPK1 stained yellow, StTMK1a sandy brown. In the ligands, oxygen atoms are colored red, nitrogen atoms are blue, phosphorus atoms are orange, carbon atoms are colored light blue in ANP and aquamarine in ATP. Mg2+ ions are represented as green spheres.CC BY · PubMed Central

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Research works printed but not linked: 3

  1. Ramavat, K., and Mérillon, J. (2014). Bulbous Plants: Biotechnology, Taylor & Francis Group.
  2. Veilleux, R.E. (1990). Haploids in Crop Improvement I, Springer.
  3. Romanov, 1989, Hormone-binding proteins of plants and the problem of perception of phytohormones, Russ. J. Plant Physiol., 36, 136

Metadata

Authors
Lomin, S. N., Kolachevskaya, O. O., Arkhipov, D. V., & Romanov, G. A.
Affiliations
Russian Academy of Sciences (RU)
Corresponding author
Romanov, Georgy A.
ORCID
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2023-07-13
Volume
24
Issue
14
Pages
11408
ISSN
1422-0067 (ISSN-L)
DOI
10.3390/ijms241411408
PMC
PMC10380454
OpenAlex
W4384341506
Cited by
3
References
109
Citations by year
2026: 1 · 2024: 1 · 2023: 1
FWCI
0.47
Type
journal article
Language
en
Open access
Licence
Locations
  • International Journal of Molecular Sciences (publishedVersion, cc-by)
  • Preprints.org (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
Russian Science Foundation (17-74-20181)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
Keywords
auxin signaling, potato, ploidy, autotetraploids, diploids, ABP1, tuberization, gene expression profiling, species specificity, Arabidopsis comparison
MeSH terms
Indoleacetic Acids, Phylogeny, Solanum tuberosum, Arabidopsis, Gene Expression Regulation, Plant, Tetraploidy

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