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Role of F-box E3-ubiquitin ligases in plant development and stress responses

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Abstract

Key message

F-box E3-ubiquitin ligases regulate critical biological processes in plant development and stress responses. Future research could elucidate why and how plants have acquired a large number of F-box genes.

Abstract

The ubiquitin–proteasome system (UPS) is a predominant regulatory mechanism employed by plants to maintain the protein turnover in the cells and involves the interplay of three classes of enzymes, E1 (ubiquitin-activating), E2 (ubiquitin-conjugating), and E3 ligases. The diverse and most prominent protein family among eukaryotes, F-box proteins, are a vital component of the multi-subunit SCF (Skp1-Cullin 1-F-box) complex among E3 ligases. Several F-box proteins with multifarious functions in different plant systems have evolved rapidly over time within closely related species, but only a small part has been characterized. We need to advance our understanding of substrate-recognition regulation and the involvement of F-box proteins in biological processes and environmental adaptation. This review presents a background of E3 ligases with particular emphasis on the F-box proteins, their structural assembly, and their mechanism of action during substrate recognition. We discuss how the F-box proteins regulate and participate in the signaling mechanisms of plant development and environmental responses. We highlight an urgent need for research on the molecular basis of the F-box E3-ubiquitin ligases in plant physiology, systems biology, and biotechnology. Further, the developments and outlooks of the potential technologies targeting the E3-ubiquitin ligases for developing crop improvement strategies have been discussed.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

Ub:

Ubiquitin

E1:

Ubiquitin-activating enzyme

E2:

Ubiquitin-conjugating enzyme

E3:

Ubiquitin ligase

RING:

Really interesting new gene

HECT:

Homology to E6-APC terminus

RBR:

RING Between RING

SKP1:

S-phase kinase-associated protein 1

RBX1:

Cullin 1- ring box-1

SCF:

Skp, Cullin, F-box containing complex or Skp1-Cullin 1-F-box

BTB:

Bric-a-brac-Tramtrack-board complex

DDB:

DNA damage-binding domain-containing

APC:

Anaphase promoting complex

ACIF:

Avr9/Cf-9-induced F-box

AFB3:

Auxin signaling F-box proteins

COI1:

Coronatine-insensitive protein 1

COS1:

COI1-suppressor1

CPR:

Constitutive expresser of PR (pathogenesis-related) genes

D3:

Dwarf3

DDF1:

Dwarf and delayed flowering 1

DIF1:

Drought-induced F-box protein 1

DOR:

Drought tolerance repressor

DRF1:

Defense-related F-box protein

EBF:

Ethylene-insensitive3 (EIN3)-binding F-box

EDL3:

Empfindlicher im dunkelroten Licht 1(EID1)-like protein 3

EID1:

Empfindlicher im dunkelroten Licht 1

EIFP1:

Erysiphe necator-induced F-box protein

EST1:

Enhanced salt tolerance 1

FBA:

F-Box-associated-domain;

FBK:

F-Box protein containing a Kelch-repeat motif

FBL:

F-box containing LRRs

FBS1:

F-Box stress-induced 1

FKF1:

Flavin-binding, Kelch-repeat, F-box

FKL:

FKF1-like protein

FOF2:

F-box of flowering 2

JAZ:

Jasmonate ZIM-domain protein

KFB1:

Kelch-repeat containing F-box protein 1

LKP:

(Light, Oxygen OR Voltage) LOV kelch protein

LTSF1:

Low-temperature-sensitive F-box1

LTSF2:

Low-temperature-sensitive F-box2

MAIF1:

MiRNAs regulated and abiotic stress-induced F-box gene

MAX2:

More axillary growth 2

MEE11:

MiRNAs regulated and abiotic stress-induced F-box gene

Msr9:

Multiple stresses responsive gene 9

ORE9:

Oresara9

PKE1:

Proline-, lysine-, and glutamic-rich protein gene 1

RIFP1:

RCAR3 (regulatory components of ABA receptor 3) interacting F-box protein 1

SAGL1:

Small and glossy leaves 1

SK1:

SKP1-like 1

SLFs:

S-locus F-box proteins

SLY1:

Protein SLEEPY

SNE1:

SNEEZY protein

SNIPER:

Snc1-influencing plant E3 ligase reverse genetic

TaCFBD:

Triticum aestivum cyclin F-box domain

TIR1:

Transport inhibitor response 1

TULP34:

Tubby-like protein genes

UCL1:

Upward curly leaf 1

UPS:

Ubiquitin proteasome system

UFO:

Unusual floral organs

VFB:

VIER F-box protein

ZTL:

Zeitlupe

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Acknowledgements

The authors would like to thank Lakshita Negi, NIFT, Shillong, India, and Henri Laugel, University of Helsinki, Finland/ UniLaSalle Beauvais, France for helping with digital art for the manuscript figures.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript. The authors declare no competing financial interests.

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Author notes

  1. Harshita Saxena and Harshita Negi have contributed equally to this work and (shared first authorship).

Authors and Affiliations

  1. Institute of Plant Breeding, Genetics, and Genomics, University of Georgia Griffin Campus, 1109 Experiment Street, Griffin, GA, 30223, USA

    Harshita Saxena

  2. Department of Biological Sciences, University of South Carolina, 715 Sumter Street, Columbia, SC, 29208, USA

    Harshita Negi

  3. School of Life and Environmental Sciences, Deakin University, Geelong Waurn Ponds Campus, Geelong, VIC, 3216, Australia

    Bhaskar Sharma

  4. Department of Botany and Plant Sciences, University of California-Riverside, Riverside, CA, 92521, USA

    Bhaskar Sharma

Authors
  1. Harshita Saxena
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Contributions

BS conceptualized and supervised the study. BS, HS, and HN collected the data and wrote the manuscript. BS critically reviewed and revised the manuscript.

Corresponding author

Correspondence to Bhaskar Sharma.

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Saxena, H., Negi, H. & Sharma, B. Role of F-box E3-ubiquitin ligases in plant development and stress responses. Plant Cell Rep 42, 1133–1146 (2023). https://doi.org/10.1007/s00299-023-03023-8

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  • DOI: https://doi.org/10.1007/s00299-023-03023-8

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