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The peptidyl-prolyl isomerases FKBP15-1 and FKBP15-2 negatively affect lateral root development by repressing the vacuolar invertase VIN2 in Arabidopsis

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Abstract

Main conclusion

The peptidyl-prolyl isomerases FKBP15-1 and FKBP15-2 negatively modulate lateral root development by repressing vacuolar invertase VIN2 activity.

Abstract

Lateral root (LR) architecture greatly affects the efficiency of nutrient absorption and the anchorage of plants. Although the internal phytohormone regulatory mechanisms that control LR development are well known, how external nutrients influence lateral root development remains elusive. Here, we characterized the function of two FK506-binding proteins, namely, FKBP15-1 and FKBP15-2, in Arabidopsis. FKBP15-1/15–2 genes were expressed prominently in the vascular bundles of the root basal meristem region, and the FKBP15-1/15–2 proteins were localized to the endoplasmic reticulum of the cells. Using IP-MS, Co-IP, and BiFC assays, we demonstrated that FKBP15-1 and FKBP15-2 interacted with vacuolar invertase 2 (VIN2). Compared to Col-0 and the single mutants, the fkbp15-1fkbp15-2 double mutant had more LRs, and presented higher sucrose catalytic activity. Moreover, genetic analysis showed genetic epistasis of VIN2 over FKBP15-1/FKBP15-2 in controlling LR development. Our results indicate that FKBP15-1 and FKBP15-2 participate in the control of LR number by inhibiting the catalytic activity of VIN2. Owing to the conserved peptidylprolyl cis–trans isomerase activity of FKBP family proteins, our results provide a clue for further analysis of the interplay between lateral root development and protein modification by FKBPs.

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Abbreviations

LR:

Lateral root

FKBP:

FK506-binding proteins

IP-MS:

Immunoprecipitation and mass spectrometry

VIN2:

Vacuolar invertase 2

XPP:

Xylem pole-pericycle

ER:

Endoplasmic reticulum

UBQ:

Ubiquitin

GUS:

ß-glucuronidase

YFP:

Yellow fluorescent protein

GFP:

Green fluorescent protein

MS:

Murashige and Skoog

TOR:

Target of rapamycin

TWD1:

TWISTED DWARF1

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Acknowledgements

This work was supported by grants from the China Transgenic Program (2019ZX08010-004). The funders were not involved in the design of the study, the data collection and analysis, or the writing of the manuscript. We thank Dr. Sheng Luan (University of California Berkeley) for kindly providing the overexpression vector. We are also grateful to the Instrument Analysis Centre of Shanghai Jiao Tong University for LC-MS/MS analysis.

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Authors and Affiliations

  1. Department of Plant Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240, China

    Jun Wang, Wenjie Sun, Xiuzhen Kong, Chunyan Zhao, Jianfu Li, Yun Chen, Zhengyin Gao & Kaijing Zuo

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  1. Jun Wang
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Correspondence to Kaijing Zuo.

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The datasets are in a publicly accessible repository

The datasets analysed for this study can be found under dataset identifiers PXD017200 and 10.6019/PXD017200 in the ProteomeXchange Consortium (https://proteomecentral.proteomexchange.org/cgi/GetDataset. Perez-Riverol et al. 2018).

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Wang, J., Sun, W., Kong, X. et al. The peptidyl-prolyl isomerases FKBP15-1 and FKBP15-2 negatively affect lateral root development by repressing the vacuolar invertase VIN2 in Arabidopsis. Planta 252, 52 (2020). https://doi.org/10.1007/s00425-020-03459-2

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