Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells

Fraysse, Laure; Wells, B.; McCann, Maureen C.; Kjellbom, Per

doi:10.1042/bc20040122

Cited by 80 publications

(58 citation statements)

References 52 publications

(77 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The target of the SE-specific antibody RS6, raised against the isolated SEs of Streptanthus tortuosus (Brassicaceae), was recently found in Arabidopsis to be an ENOD-like integral protein (Khan et al, 2007). Other proteins have been immunolocalized to SEs, such as the Suc-H 1 symporter SUT1 in potato (Solanum tuberosum; Kü hn et al, 1997), a putative monosaccharide transporter and a protonATPase in developing apple (Malus domestica) fruit (Zhang et al, 2004), a proton-amino acid transporter in Arabidopsis roots (Okumoto et al, 2004), a calcium channel-like protein in tobacco and Pistia stratiotes leaves (Volk and Franceschi, 2000), and a plasma membrane aquaporin in spinach (Spinacia oleracea; Fraysse et al, 2005).…”

Section: Expression Of the Sumcr Construct Yields An Mcitrine Signal mentioning

confidence: 99%

“…The strong CC-specific promoter AtSUC2p (Truernit and Sauer, 1995;Imlau et al, 1999) was used to drive FP fusions (Cutler et al, 2000) of proteins that are known to be targeted to plasma membranes (PIP subfamily of aquaporins; Fraysse et al, 2005) or are potentially small enough to sneak through the plasmodesmata as an FP fusion (AtRCI2A and AtRCI2B; Medina et al, 2001;Nylander et al, 2001). N-terminal FP fusions were employed to avoid interruption of potentially important 3#-signaling sequences in the mature mRNA, and a monomeric, environmentally stable form of yellow fluorescent protein (YFP; mCitrine) was used to avoid FP dimerization (Griesbeck et al, 2001;Zacharias et al, 2002).…”

mentioning

confidence: 99%

See 1 more Smart Citation

A Plasma Membrane-Anchored Fluorescent Protein Fusion Illuminates Sieve Element Plasma Membranes in Arabidopsis and Tobacco

Thompson

Wolniak

2008

Plant Physiology

View full text Add to dashboard Cite

Rapid acquisition of quantitative anatomical data from the sieve tubes of angiosperm phloem has been confounded by their small size, their distance from organ surfaces, and the time-consuming nature of traditional methods, such as transmission electron microscopy. To improve access to these cells, for which good anatomical data are critical, a monomeric yellow fluorescent protein (mCitrine) was N-terminally fused to a small (approximately 6 kD) membrane protein (AtRCI2A) and stably expressed in Arabidopsis thaliana (Columbia-0 ecotype) and Nicotiana tabacum (‘Samsun’) under the control of a companion cell-specific promoter (AtSUC2p). The construct, called by its abbreviation SUmCR, yielded stable sieve element (SE) plasma membrane fluorescence labeling, even after plastic (methacrylate) embedding. In conjunction with wide-field fluorescence measurements of sieve pore number and position using aniline blue-stained callose, mCitrine-labeled material was used to calculate rough estimates of sieve tube-specific conductivity for both species. The SUmCR construct also revealed a hitherto unknown expression domain of the AtSUC2 Suc-H+ symporter in the epidermis of the cell division zone of developing root tips. The success of this construct in targeting plasma membrane-anchored fluorescent proteins to SEs could be attributable to the small size of AtRCI2A or to the presence of other signals innate to AtRCI2A that permit the protein to be trafficked to SEs. The construct provides a hitherto unique entrée into companion cell-to-SE protein targeting, as well as a new tool for studying whole-plant phloem anatomy and architecture.

show abstract

Section: Expression Of the Sumcr Construct Yields An Mcitrine Signal mentioning

confidence: 99%

mentioning

confidence: 99%

A Plasma Membrane-Anchored Fluorescent Protein Fusion Illuminates Sieve Element Plasma Membranes in Arabidopsis and Tobacco

Thompson

Wolniak

2008

Plant Physiology

View full text Add to dashboard Cite

show abstract

“…Antisense inhibition experiments on Arabidopsis thaliana PIP1 and PIP2 have suggested that the two subgroups of aquaporins contribute to root or leaf hydraulic conductivity in the same way (13). In several plant species, members of the PIP1 and PIP2 subgroups were shown to be coexpressed in the same cell type (14)(15)(16)(17).…”

mentioning

confidence: 99%

Heteromerization of PIP aquaporins affects their intrinsic permeability

Yaneff

Sigaut

Marquez

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

101

View full text Add to dashboard Cite

The plant aquaporin plasma membrane intrinsic proteins (PIP) subfamily represents one of the main gateways for water exchange at the plasma membrane (PM). A fraction of this subfamily, known as PIP1, does not reach the PM unless they are coexpressed with a PIP2 aquaporin. Although ubiquitous and abundantly expressed, the role and properties of PIP1 aquaporins have therefore remained masked. Here, we unravel how FaPIP1;1, a fruit-specific PIP1 aquaporin from Fragaria x ananassa, contributes to the modulation of membrane water permeability (P f ) and pH aquaporin regulation. Our approach was to combine an experimental and mathematical model design to test its activity without affecting its trafficking dynamics. We demonstrate that FaPIP1;1 has a high water channel activity when coexpressed as well as how PIP1-PIP2 affects gating sensitivity in terms of cytosolic acidification. PIP1-PIP2 random heterotetramerization not only allows FaPIP1;1 to arrive at the PM but also produces an enhancement of FaPIP2;1 activity. In this context, we propose that FaPIP1;1 is a key participant in the regulation of water movement across the membranes of cells expressing both aquaporins.T he plasma membrane (PM) is the first barrier that limits water exchange in plant cells. The rate of its water transport capacity is mainly associated with aquaporins. Among the seven aquaporin subfamilies described in the plant kingdom, only plasma membrane intrinsic proteins (PIP) and some members of the nodulin-26-like intrinsic proteins (NIP) and X intrinsic proteins (XIP) subfamilies have been shown to be preferentially localized at the PM (1, 2). Of these, PIP aquaporins appear to have a large role in controlling membrane water permeability, whereas NIP and XIP have been mainly described as solute transporters (2-4). Plant PIP aquaporins represent a conserved subfamily that has been historically divided into two subgroups due to their differences in primary structure, PIP1 and PIP2. Interestingly, PIP aquaporins compose ∼40% of the total aquaporin set, and the PIP1 and PIP2 ratio among different species is relatively constant (5-12). Fig. S1 shows the distribution of all aquaporin genes present in plants whose genome has been completely sequenced and analyzed. Antisense inhibition experiments on Arabidopsis thaliana PIP1 and PIP2 have suggested that the two subgroups of aquaporins contribute to root or leaf hydraulic conductivity in the same way (13). In several plant species, members of the PIP1 and PIP2 subgroups were shown to be coexpressed in the same cell type (14-17).Although PIP1 are as ubiquitous as PIP2, the functional properties of each type of channel are different. PIP2 are very well described as a homotetramer with high water transport activity (18, 19) and a gating mechanism unequivocally associated with specific and conserved amino acid motifs triggered by cytosolic acidification (20-22), phosphorylation (23, 24), or divalent cation concentration (22). In contrast, PIP1 have shown complex heterogeneity in water and solute transpor...

show abstract

“…However, it has remained unclear whether the accompanying water flow across the guard cell plasma membrane and tonoplast can simply be mediated by the lipid phase of membranes or whether aquaporins, channel proteins that facilitate transmembrane water transport, are involved. In fact, information on aquaporin expression in guard cells has remained scarce (Sarda et al, 1997;Sun et al, 2001;Fraysse et al, 2005;Shope and Mott, 2006;Yang et al, 2006;Heinen et al, 2014). Plasma membrane intrinsic proteins (PIPs) represent the most abundant aquaporins in the plant plasma membrane (Santoni et al, 2003), and transcriptome analysis indicated expression of 8 and 12 PIP isoforms in stomata of Arabidopsis thaliana and stomatal complexes of maize (Zea mays), respectively (Leonhardt et al, 2004;Heinen et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Aquaporins Contribute to ABA-Triggered Stomatal Closure through OST1-Mediated Phosphorylation

et al. 2015

View full text Add to dashboard Cite

International audienceStomatal movements in response to environmental stimuli critically control the plant water status. Although these movements are governed by osmotically driven changes in guard cell volume, the role of membrane water channels (aquaporins) has remained hypothetical. Assays in epidermal peels showed that knockout Arabidopsis thaliana plants lacking the Plasma membrane Intrinsic Protein 2;1 (PIP2;1) aquaporin have a defect in stomatal closure, specifically in response to abscisic acid (ABA). ABA induced a 2-fold increase in osmotic water permeability (Pf) of guard cell protoplasts and an accumulation of reactive oxygen species in guard cells, which were both abrogated in pip2;1 plants. Open stomata 1 (OST1)/Snf1-related protein kinase 2.6 (SnRK2.6), a protein kinase involved in guard cell ABA signaling, was able to phosphorylate a cytosolic PIP2;1 peptide at Ser-121. OST1 enhanced PIP2;1 water transport activity when coexpressed in Xenopus laevis oocytes. Upon expression in pip2;1 plants, a phosphomimetic form (Ser121Asp) but not a phosphodeficient form (Ser121Ala) of PIP2;1 constitutively enhanced the Pf of guard cell protoplasts while suppressing its ABA-dependent activation and was able to restore ABA-dependent stomatal closure in pip2;1. This work supports a model whereby ABA-triggered stomatal closure requires an increase in guard cell permeability to water and possibly hydrogen peroxide, through OST1-dependent phosphorylation of PIP2;1 at Ser-121

show abstract

Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells

Abstract: Localization of the two abundant aquaporin isoforms suggests roles for specific PIPs of the PIP1 subgroup in phloem loading, transport and unloading, and in stomatal movements.

Cited by 80 publications

References 52 publications

A Plasma Membrane-Anchored Fluorescent Protein Fusion Illuminates Sieve Element Plasma Membranes in Arabidopsis and Tobacco

A Plasma Membrane-Anchored Fluorescent Protein Fusion Illuminates Sieve Element Plasma Membranes in Arabidopsis and Tobacco

Heteromerization of PIP aquaporins affects their intrinsic permeability

Aquaporins Contribute to ABA-Triggered Stomatal Closure through OST1-Mediated Phosphorylation

Contact Info

Product

Resources

About