Tonoplast Aquaporins Facilitate Lateral Root Emergence.

Hagen Reinhardt,Kamal Swarup,Charles Hachez,Malcolm J Bennett,Karim Bouhidel,Ute Voß,Azeez Beebo,Manuela Désirée Bienert,Jan K Schjoerring,Lorenzo Frigerio,Francois Chaumont

doi:10.1104/pp.15.01635

Abstract

Aquaporins (AQPs) are water channels allowing fast and passive diffusion of water across cell membranes. It was hypothesized that AQPs contribute to cell elongation processes by allowing water influx across the plasma membrane and the tonoplast to maintain adequate turgor pressure. Here, we report that, in Arabidopsis (Arabidopsis thaliana), the highly abundant tonoplast AQP isoforms AtTIP1;1, AtTIP1;2, and AtTIP2;1 facilitate the emergence of new lateral root primordia (LRPs). The number of lateral roots was strongly reduced in the triple tip mutant, whereas the single, double, and triple tip mutants showed no or minor reduction in growth of the main root. This phenotype was due to the retardation of LRP emergence. Live cell imaging revealed that tight spatiotemporal control of TIP abundance in the tonoplast of the different LRP cells is pivotal to mediating this developmental process. While lateral root emergence is correlated to a reduction of AtTIP1;1 and AtTIP1;2 protein levels in LRPs, expression of AtTIP2;1 is specifically needed in a restricted cell population at the base, then later at the flanks, of developing LRPs. Interestingly, the LRP emergence phenotype of the triple tip mutants could be fully rescued by expressing AtTIP2;1 under its native promoter. We conclude that TIP isoforms allow the spatial and temporal fine-tuning of cellular water transport, which is critically required during the highly regulated process of LRP morphogenesis and emergence.

Highlights

Aquaporins (AQPs) are water channels allowing fast and passive diffusion of water across cell membranes
The genome of Arabidopsis (Arabidopsis thaliana) encodes 35 major intrinsic proteins that phylogenetically cluster in four subfamilies: plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), small basic intrinsic proteins, and nodulin 26-like intrinsic proteins (Johanson et al, 2001)
The T-DNA and defective Suppressor-mutator insertions in single tip1;1, tip1;2, and tip2;1 mutants are illustrated in Supplemental Figure S1 (A, B, and C, respectively)

Summary

Introduction

Aquaporins (AQPs) are water channels allowing fast and passive diffusion of water across cell membranes. Plant cell elongation is a developmental process during which cells increase 10- to 100-fold in volume before reaching their final size It requires a fast and continuous inflow of water, which ends up mainly in the vacuole, in a process that is controlled by gradients in water potential, which itself is generated by the accumulation of solutes (for review, see Fricke and Chaumont, 2007). AQPs are involved, on the one hand, in the long-distance movement of water during evapo-transpiration and, on the other hand, in the short-distance transport and osmotic adjustment within cells (expansion, opening of stomata, water homeostasis; Maurel et al, 2008; Gomes et al, 2009; Heinen et al, 2009; Chaumont and Tyerman, 2014) They contribute to the maintenance of a favorable water balance within plants under changing and sometimes hostile environmental conditions. Some clues come from the overexpression of the cauliflower (Brassica oleracea) or tobacco (Nicotiana tabacum) TIP1;1 gene in tobacco suspension cells, which results in an increase in cell growth and size (Reisen et al, 2003; Okubo-Kurihara et al, 2009)

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Conclusion