Endoplasmic Reticulum-Localized PURINE PERMEASE1 Regulates Plant Height and Grain Weight by Modulating Cytokinin Distribution in Rice

Abstract

Cytokinins (CKs) are a class of phytohormones playing essential roles in various biological processes. However, the mechanisms underlying CK transport as well as its function in plant growth and development are far from being fully elucidated. Here, we characterize the function of PURINE PERMEASE1 (OsPUP1) in rice (Oryza sativa L.). OsPUP1 was predominantly expressed in the root, particularly in vascular cells, and CK treatment can induce its expression. Subcellular localization analysis showed that OsPUP1 was predominantly localized to the endoplasmic reticulum (ER). Overexpression of OsPUP1 resulted in growth defect of various aerial tissues, including decreased leaf length, plant height, grain weight, panicle length, and grain number. Hormone profiling revealed that the CK content was decreased in the shoot of OsPUP1-overexpressing seedling, but increased in the root, compared with the wild type. The CK content in the panicle was also decreased. Quantitative reverse transcription-PCR (qRT-PCR) analysis using several CK type-A response regulators (OsRRs) as the marker genes suggested that the CK response in the shoot of OsPUP1-overexpressing seedling is decreased compared to the wild type when CKs are applied to the root. Genetic analysis revealed that BG3/OsPUP4, a putative plasma membrane-localized CK transporter, overcomes the function of OsPUP1. We hypothesize that OsPUP1 might be involved in importing CKs into ER to unload CKs from the vascular tissues by cell-to-cell transport.

Integrating the Roles for Cytokinin and Auxin in De Novo Shoot Organogenesis: From Hormone Uptake to Signaling Outputs

“…The rice PUP family has 13 members (OsPUP1-OsPUP13), of which OsPUP1, OsPUP4 and OsPUP7 function as CK transporters. Interestingly, only OsPUP4 localizes to the PM, whereas OsPUP1 and OsPUP7 localize to the ER [211,212].…”

“…New insights into CK perception suggest a relevance of both ER-based and PM-based CK signaling in plants [145,146]. Furthermore, multiple reports on the presence of purine transporters on the ER [211,212,214] have opened new possibilities for the interpretation of CK flow through plant tissues. According to the proposed interpretation, the lumen of the ER represents a novel domain for CK action, equipped with elements of CK perception, metabolism, transport and signaling that are equivalent but not identical to the ones present in the apoplast.…”

Conservation and divergence: Regulatory networks underlying reproductive branching in rice and maize

“…In general, root-derived CKs are transported to shoots via efflux and influx carriers: equilibrative nucleotide transporter (ENT), purine permease (PUP), and three ATP-binding cassette G (ABCG) transporter families. OsENT2 [79] , OsPUP1 , 4 , 7 , [80] , [81] , [82] and OsABCG18 [83] are considered as the long-distance transporters of the root-derived CKs, transporting them towards the shoot and modulate tiller numbers, panicle branches, and grain yield by transporting tZ-type CKs ( Fig. 3 D; Supplemental table 1 ).…”

Functional identification of purine permeases reveals their roles in caffeine transport in tea plants (Camellia sinensis)

“…It was inferred that OsPUP4 and OsPUP7 function synergistically as cytokinin transporters in its long-distance movement and local allocation ( Xiao et al., 2018 ). OsPUP1 was also localized on ER and could import cytokinins from the vascular tissues by cell-to-cell transport ( Xiao et al., 2020 ). NtNUP1 (nicotine uptake permease), which belongs to PUPs family in tobacco, was demonstrated to transport various compounds in yeast system.…”