The peptidyl-prolyl isomerases FKBP15-1 and FKBP15-2 negatively affect lateral root development by repressing the vacuol

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ORIGINAL ARTICLE

The peptidyl‑prolyl isomerases FKBP15‑1 and FKBP15‑2 negatively affect lateral root development by repressing the vacuolar invertase VIN2 in Arabidopsis Jun Wang1 · Wenjie Sun1 · Xiuzhen Kong1 · Chunyan Zhao1 · Jianfu Li1 · Yun Chen1 · Zhengyin Gao1 · Kaijing Zuo1  Received: 15 April 2020 / Accepted: 11 September 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

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. Keywords  Arabidopsis · Lateral root · FKBP15-1/FKBP15-2 · VIN2 · Sucrose 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

Communicated by Anastasios Melis.

Introduction

Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0042​5-020-03459​-2) contains supplementary material, which is available to authorized users. * Kaijing Zuo [email protected] 1



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

Lateral roots (LRs) contribute to the plant root system and are important for nutrient and water uptake as well as physical anchorage (Tian et al. 2014). To meet the demands of plant growth, most plant species must possess well-developed LRs to increase the root space in soil (McCleery et al. 2017). Plants with well-de