The CBL-Interacting Protein Kinase CIPK23 Regulates HAK5-Mediated High-Affinity K⁺ Uptake in Arabidopsis Roots

Plant growth and development requires efficient acquisition of essential elements. Potassium (K⁺) is an important macronutrient present in the soil solution at a wide range of concentrations. Regulation of the K⁺ uptake systems in the roots is essential to secure K⁺ supply. It has been shown in Arab...

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Veröffentlicht in:Plant physiology (Bethesda) 2015-12, Vol.169 (4), p.2863-2873
Hauptverfasser: Ragel, Paula, Ródenas, Reyes, García-Martín, Elena, Andrés, Zaida, Villalta, Irene, Nieves-Cordones, Manuel, Rivero, Rosa M., Martínez, Vicente, Pardo, Jose M., Quintero, Francisco J., Rubio, Francisco
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container_title Plant physiology (Bethesda)
container_volume 169
creator Ragel, Paula
Ródenas, Reyes
García-Martín, Elena
Andrés, Zaida
Villalta, Irene
Nieves-Cordones, Manuel
Rivero, Rosa M.
Martínez, Vicente
Pardo, Jose M.
Quintero, Francisco J.
Rubio, Francisco
description Plant growth and development requires efficient acquisition of essential elements. Potassium (K⁺) is an important macronutrient present in the soil solution at a wide range of concentrations. Regulation of the K⁺ uptake systems in the roots is essential to secure K⁺ supply. It has been shown in Arabidopsis (Arabidopsis thaliana) that when the external K⁺ concentration is very low (
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Potassium (K⁺) is an important macronutrient present in the soil solution at a wide range of concentrations. Regulation of the K⁺ uptake systems in the roots is essential to secure K⁺ supply. It has been shown in Arabidopsis (Arabidopsis thaliana) that when the external K⁺ concentration is very low (&lt;10μM), K⁺ nutrition depends exclusively on the high-affinity K⁺ transporter5 (HAK5). Low-K⁺-induced transcriptional activation of the gene encoding HAK5 has been previously reported. Here, we show the posttranscriptional regulation of HAK5 transport activity by phosphorylation. Expression in a heterologous system showed that the Ca²⁺ sensors calcineurin B-like (CBL1), CBL8, CBL9, and CBL10, together with CBL-interacting protein kinase23 (CIPK23), activated HAK5 in vivo. This activation produced an increase in the affinity and theV maxof K⁺ transport. In vitro experiments show that the N terminus of HAK5 is phosphorylated by CIPK23. This supports the idea that phosphorylation of HAK5 induces a conformational change that increases its affinity for K⁺. Experiments of K⁺ (Rb⁺) uptake and growth measurements in low-K⁺ medium with Arabidopsis single mutantshak5, akt1, andcipk23, double mutantshak5 akt1, hak5 cipk23, andakt1 cipk23, and the triple mutanthak5 akt1 cipk23confirmed the regulatory role of CIPK23 in planta.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.15.01401</identifier><identifier>PMID: 26474642</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Binding, Competitive ; Calcium-Binding Proteins - genetics ; Calcium-Binding Proteins - metabolism ; Cell growth ; Gene expression regulation ; Ion Transport ; Kinetics ; Life Sciences ; MEMBRANES, TRANSPORT, AND BIOENERGETICS ; Mutation ; Phosphorylation ; Plant growth ; Plant growth regulators ; Plant roots ; Plant Roots - genetics ; Plant Roots - metabolism ; Plants ; Potassium ; Potassium - metabolism ; Potassium-Hydrogen Antiporters - genetics ; Potassium-Hydrogen Antiporters - metabolism ; Protein Binding ; Protein-Serine-Threonine Kinases - genetics ; Protein-Serine-Threonine Kinases - metabolism ; Proteins ; Rubidium - metabolism ; Two-Hybrid System Techniques ; Vegetal Biology ; Yeasts</subject><ispartof>Plant physiology (Bethesda), 2015-12, Vol.169 (4), p.2863-2873</ispartof><rights>Copyright © 2015 American Society of Plant Biologists</rights><rights>2015 American Society of Plant Biologists. All Rights Reserved.</rights><rights>Attribution</rights><rights>2015 American Society of Plant Biologists. All Rights Reserved. 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-ff6f01831f9bf97effa5480ac8a179a58f8a48a92d6267d0b578270e97f151ef3</citedby><orcidid>0000-0001-8718-2975 ; 0000-0003-3880-0241 ; 0000-0003-4510-8624 ; 0000-0001-7640-9548 ; 0000-0002-8698-0833 ; 0000-0002-3754-9609</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/planphys.169.4.2863$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/planphys.169.4.2863$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,27915,27916,58008,58241</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26474642$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01595629$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Ragel, Paula</creatorcontrib><creatorcontrib>Ródenas, Reyes</creatorcontrib><creatorcontrib>García-Martín, Elena</creatorcontrib><creatorcontrib>Andrés, Zaida</creatorcontrib><creatorcontrib>Villalta, Irene</creatorcontrib><creatorcontrib>Nieves-Cordones, Manuel</creatorcontrib><creatorcontrib>Rivero, Rosa M.</creatorcontrib><creatorcontrib>Martínez, Vicente</creatorcontrib><creatorcontrib>Pardo, Jose M.</creatorcontrib><creatorcontrib>Quintero, Francisco J.</creatorcontrib><creatorcontrib>Rubio, Francisco</creatorcontrib><title>The CBL-Interacting Protein Kinase CIPK23 Regulates HAK5-Mediated High-Affinity K⁺ Uptake in Arabidopsis Roots</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Plant growth and development requires efficient acquisition of essential elements. Potassium (K⁺) is an important macronutrient present in the soil solution at a wide range of concentrations. Regulation of the K⁺ uptake systems in the roots is essential to secure K⁺ supply. It has been shown in Arabidopsis (Arabidopsis thaliana) that when the external K⁺ concentration is very low (&lt;10μM), K⁺ nutrition depends exclusively on the high-affinity K⁺ transporter5 (HAK5). Low-K⁺-induced transcriptional activation of the gene encoding HAK5 has been previously reported. Here, we show the posttranscriptional regulation of HAK5 transport activity by phosphorylation. Expression in a heterologous system showed that the Ca²⁺ sensors calcineurin B-like (CBL1), CBL8, CBL9, and CBL10, together with CBL-interacting protein kinase23 (CIPK23), activated HAK5 in vivo. This activation produced an increase in the affinity and theV maxof K⁺ transport. In vitro experiments show that the N terminus of HAK5 is phosphorylated by CIPK23. This supports the idea that phosphorylation of HAK5 induces a conformational change that increases its affinity for K⁺. Experiments of K⁺ (Rb⁺) uptake and growth measurements in low-K⁺ medium with Arabidopsis single mutantshak5, akt1, andcipk23, double mutantshak5 akt1, hak5 cipk23, andakt1 cipk23, and the triple mutanthak5 akt1 cipk23confirmed the regulatory role of CIPK23 in planta.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Binding, Competitive</subject><subject>Calcium-Binding Proteins - genetics</subject><subject>Calcium-Binding Proteins - metabolism</subject><subject>Cell growth</subject><subject>Gene expression regulation</subject><subject>Ion Transport</subject><subject>Kinetics</subject><subject>Life Sciences</subject><subject>MEMBRANES, TRANSPORT, AND BIOENERGETICS</subject><subject>Mutation</subject><subject>Phosphorylation</subject><subject>Plant growth</subject><subject>Plant growth regulators</subject><subject>Plant roots</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - metabolism</subject><subject>Plants</subject><subject>Potassium</subject><subject>Potassium - metabolism</subject><subject>Potassium-Hydrogen Antiporters - genetics</subject><subject>Potassium-Hydrogen Antiporters - metabolism</subject><subject>Protein Binding</subject><subject>Protein-Serine-Threonine Kinases - genetics</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Proteins</subject><subject>Rubidium - metabolism</subject><subject>Two-Hybrid System Techniques</subject><subject>Vegetal Biology</subject><subject>Yeasts</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUtvEzEQxy0EomnhxB35CIcNttfPC9ISURIliKpqz5aza2ddNmt37VTKka_Fx-GTYNRSHqd5_Gd-M6MB4BVGc4wRfRfjHLM5whThJ2CGWU0qwqh8CmYIFR9JqU7AaUo3CCFcY_ocnBBOBeWUzEC86i1cfNhUqzHbybTZjzt4MYVs_QjXfjSpyKuLNanhpd0dBpNtgstmzarPtvMl6uDS7_qqcc6PPh_h-se37_A6ZvPVwoJoJrP1XYjJJ3gZQk4vwDNnhmRfPtgzcH3-8WqxrDZfPq0WzaZqa8Fy5Rx3CMsaO7V1SljnTLkJmVYaLJRh0klDpVGk44SLDm2ZkEQgq4TDDFtXn4H399x42O5t19oxT2bQcfJ7Mx11MF7_q4y-17twpykXQmFRAG_vAf1_bctmo3_lEGaKcaLucKl98zBsCrcHm7Le-9TaYTCjDYeksaCKE0QoK6Wv_97rkfz7JX9YNymH6VGPhRX7Y2Fxpakmktf1T_5qm0E</recordid><startdate>20151201</startdate><enddate>20151201</enddate><creator>Ragel, Paula</creator><creator>Ródenas, Reyes</creator><creator>García-Martín, Elena</creator><creator>Andrés, Zaida</creator><creator>Villalta, Irene</creator><creator>Nieves-Cordones, Manuel</creator><creator>Rivero, Rosa M.</creator><creator>Martínez, Vicente</creator><creator>Pardo, Jose M.</creator><creator>Quintero, Francisco J.</creator><creator>Rubio, Francisco</creator><general>American Society of Plant Biologists</general><general>Oxford University Press ; 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Potassium (K⁺) is an important macronutrient present in the soil solution at a wide range of concentrations. Regulation of the K⁺ uptake systems in the roots is essential to secure K⁺ supply. It has been shown in Arabidopsis (Arabidopsis thaliana) that when the external K⁺ concentration is very low (&lt;10μM), K⁺ nutrition depends exclusively on the high-affinity K⁺ transporter5 (HAK5). Low-K⁺-induced transcriptional activation of the gene encoding HAK5 has been previously reported. Here, we show the posttranscriptional regulation of HAK5 transport activity by phosphorylation. Expression in a heterologous system showed that the Ca²⁺ sensors calcineurin B-like (CBL1), CBL8, CBL9, and CBL10, together with CBL-interacting protein kinase23 (CIPK23), activated HAK5 in vivo. This activation produced an increase in the affinity and theV maxof K⁺ transport. In vitro experiments show that the N terminus of HAK5 is phosphorylated by CIPK23. This supports the idea that phosphorylation of HAK5 induces a conformational change that increases its affinity for K⁺. Experiments of K⁺ (Rb⁺) uptake and growth measurements in low-K⁺ medium with Arabidopsis single mutantshak5, akt1, andcipk23, double mutantshak5 akt1, hak5 cipk23, andakt1 cipk23, and the triple mutanthak5 akt1 cipk23confirmed the regulatory role of CIPK23 in planta.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>26474642</pmid><doi>10.1104/pp.15.01401</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0001-8718-2975</orcidid><orcidid>https://orcid.org/0000-0003-3880-0241</orcidid><orcidid>https://orcid.org/0000-0003-4510-8624</orcidid><orcidid>https://orcid.org/0000-0001-7640-9548</orcidid><orcidid>https://orcid.org/0000-0002-8698-0833</orcidid><orcidid>https://orcid.org/0000-0002-3754-9609</orcidid><oa>free_for_read</oa></addata></record>
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ispartof Plant physiology (Bethesda), 2015-12, Vol.169 (4), p.2863-2873
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subjects Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Binding, Competitive
Calcium-Binding Proteins - genetics
Calcium-Binding Proteins - metabolism
Cell growth
Gene expression regulation
Ion Transport
Kinetics
Life Sciences
MEMBRANES, TRANSPORT, AND BIOENERGETICS
Mutation
Phosphorylation
Plant growth
Plant growth regulators
Plant roots
Plant Roots - genetics
Plant Roots - metabolism
Plants
Potassium
Potassium - metabolism
Potassium-Hydrogen Antiporters - genetics
Potassium-Hydrogen Antiporters - metabolism
Protein Binding
Protein-Serine-Threonine Kinases - genetics
Protein-Serine-Threonine Kinases - metabolism
Proteins
Rubidium - metabolism
Two-Hybrid System Techniques
Vegetal Biology
Yeasts
title The CBL-Interacting Protein Kinase CIPK23 Regulates HAK5-Mediated High-Affinity K⁺ Uptake in Arabidopsis Roots
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