Potassium transporter KUP9 participates in K+ distribution in roots and leaves under low K+ stress

Taro Yamanashi, Takeshi Uchiyama, Shunya Saito, Taiki Higashi, Hayato Ikeda, Hidetoshi Kikunaga, Mutsumi Yamagami, Yasuhiro Ishimaru, Nobuyuki Uozumi

Stress Biology ›› 2022, Vol. 2 ›› Issue (1) : 52. DOI: 10.1007/s44154-022-00074-x
Original Paper

Potassium transporter KUP9 participates in K+ distribution in roots and leaves under low K+ stress

Author information +
History +

Abstract

Potassium (K) is a major essential element in plant cells, and KUP/HAK/KT-type K+ transporters participate in the absorption of K+ into roots and in the long-distance transport to above-ground parts. In Arabidopsis thaliana, KUP9 is involved in the transport of K+ and Cs+ in roots. In this study, we investigated KUP9 function in relation to the K+ status of the plant. The expression of KUP9 was upregulated in older leaves on K+-depleted medium, compared to the expression of the other 12 KUP genes in the KUP/HAK/KT family in Arabidopsis. When grown on low K+ medium, the kup9 mutant had reduced chlorophyll content in seedlings and chlorosis in older rosette leaves. Tissue-specific expression of KUP9 determined by KUP9 promoter:GUS assay depended on the K+ status of the plants: In K+ sufficient medium, KUP9 was expressed in the leaf blade towards the leaf tip, whereas in K+ depleted medium expression was mainly found in the petioles. In accordance with this, K+ accumulated in the roots of kup9 plants. The short-term 43K+ tracer measurement showed that 43K was transferred at a lower rate in roots and shoots of kup9, compared to the wild type. These data show that KUP9 participates in the distribution of K+ in leaves and K+ absorption in roots under low K+ conditions.

Keywords

Potassium / KUP9 / Arabidopsis thaliana / KUP/HAK/KT

Cite this article

Download citation ▾
Taro Yamanashi, Takeshi Uchiyama, Shunya Saito, Taiki Higashi, Hayato Ikeda, Hidetoshi Kikunaga, Mutsumi Yamagami, Yasuhiro Ishimaru, Nobuyuki Uozumi. Potassium transporter KUP9 participates in K+ distribution in roots and leaves under low K+ stress. Stress Biology, 2022, 2(1): 52 https://doi.org/10.1007/s44154-022-00074-x

References

[1]
AdamsE, AbdollahiP, ShinR. Cesium inhibits plant growth through jasmonate signaling in Arabidopsis thaliana. Int J Mol Sci, 2013, 14: 4545-4559
CrossRef Google scholar
[2]
Adams E, Miyazaki T, Saito S, Uozumi N, Shin R (2019a) Cesium inhibits plant growth primarily through reduction of potassium influx and accumulation in Arabidopsis. Plant Cell Physiol 60:63–76. https://doi.org/10.1093/pcp/pcy188
[3]
AdamsE, MiyazakiT, ShinR. Contribution of KUPs to potassium and cesium accumulation appears complementary in Arabidopsis. Plant Signal Behav, 2019, 14: 1-3
CrossRef Google scholar
[4]
AhnSJ, ShinR, SchachtmanDP. Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake. Plant Physiol, 2004, 134: 1135-1145
CrossRef Google scholar
[5]
Alemán F, Caballero F, Ródenas R, Rivero RM, Martínez V, Rubio F (2014) The F130S point mutation in the Arabidopsis high-affinity K+ transporter AtHAK5 increases K+ over Na+ and Cs+ selectivity and confers Na+ and Cs+ tolerance to yeast under heterologous expression. Front Plant Sci 5:1–11. https://doi.org/10.3389/fpls.2014.00430
[6]
Al-Younis I, Wong A, Lemtiri-Chlieh F, Schmöckel S, Tester M, Gehring C et al (2018) The Arabidopsis thaliana K+ −uptake permease 5 (AtKUP5) contains a functional cytosolic adenylate cyclase essential for K+ transport. Front Plant Sci 871:1–15. https://doi.org/10.3389/fpls.2018.01645
[7]
DreyerI, Gomez-porrasJL, RiedelsbergerJ. The potassium battery: a mobile energy source for transport processes in plant vascular tissues. New Phytol, 2017, 216: 1049-1053
CrossRef Google scholar
[8]
FuHH, LuanS. AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell, 1998, 10: 63-73
CrossRef Google scholar
[9]
GambaleF, UozumiN. Properties of shaker-type potassium channels in higher plants. J Membr Biol, 2006, 210: 1-19
CrossRef Google scholar
[10]
Genies L, Orjollet D, Carasco L, Camilleri V, Frelon S, Vavasseur A et al (2017) Uptake and translocation of cesium by Arabidopsis thaliana in hydroponics conditions: links between kinetics and molecular mechanisms. Environ Exp Bot 138:164–172. https://doi.org/10.1016/j.envexpbot.2017.03.013
[11]
Genies L, Martin L, Kanno S, Chiarenza S, Carasco L, Camilleri V et al (2021) Disruption of AtHAK/KT/KUP9 enhances plant cesium accumulation under low potassium supply. Physiol Plant 173:1230–1243. https://doi.org/10.1111/ppl.13518
[12]
GierthM, MäserP. Potassium transporters in plants - involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett, 2007, 581: 2348-2356
CrossRef Google scholar
[13]
GierthM, MäserP, SchroederJI. The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol, 2005, 137: 1105-1114
CrossRef Google scholar
[14]
HanM, WuW, WuWH, WangY. Potassium transporter KUP7 is involved in K+ acquisition and translocation in arabidopsis rroot under K+-limited conditions. Mol Plant, 2016, 9: 437-446
CrossRef Google scholar
[15]
Hasanuzzaman M, Bhuyan MHMB, Nahar K,  Hossain MS, Mahmud JA, Hossen MS et al (2018) Potassium: a vital regulator of plant responses and tolerance to abiotic stresses. Agronomy 8:31. https://doi.org/10.3390/agronomy8030031
[16]
Held K, Pascaud F, Eckert C, Gajdanowicz P, Hashimoto K, Corratgé-Faillie C et al (2011) Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res 21:1116–1130. https://doi.org/10.1038/cr.2011.50
[17]
Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F, Porée F et al (2003) The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci U S A 100:5549–5554. https://doi.org/10.1073/pnas.0733970100
[18]
JeffersonRA, KavanaghTA, BevanMW. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J, 1987, 6: 3901-3907
CrossRef Google scholar
[19]
Kanter U, Hauser A, Michalke B, Dräxl S, Schäffner AR (2010) Caesium and strontium accumulation in shoots of Arabidopsis thaliana: genetic and physiological aspects. J Exp Bot 61:3995–4009. https://doi.org/10.1093/jxb/erq213
[20]
KimEJ, KwakJM, UozumiN, SchroederJI. AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell, 1998, 10: 51-62
CrossRef Google scholar
[21]
KobayashiD, UozumiN, HisamatsuS, YamagamiM. AtKUP/HAK/KT9, a K+ transporter from Arabidopsis thaliana, mediates Cs+ uptake in Escherichia coli. Biosci Biotechnol Biochem, 2010, 74: 203-205
CrossRef Google scholar
[22]
Lee SC, Lan WZ, Kim BG, Li L, Cheong YH, Pandey GK et al (2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc Natl Acad Sci U S A 104:15959–15964. https://doi.org/10.1073/pnas.0707912104
[23]
MaríaAB, RonaldDK, SusanJAB, AlonsoRN. A potassium transporter of the yeast Schwanniomyces occidentalis homologous to the Kup system of Escherichia coli has a high concentrative capacity. EMBO J, 1995, 14: 3021-3027
CrossRef Google scholar
[24]
Mouline K, Véry AA, Gaymard F, Boucherez J, Pilot G, Devic M et al (2002) Pollen tube development and competitive ability are impaired by disruption of a shaker K+ channel in Arabidopsis. Genes Dev 16:339–350. https://doi.org/10.1101/gad.213902
[25]
Nieves-CordonesM, AlemánF, MartínezV, RubioF. The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions. Mol Plant, 2010, 3: 326-333
CrossRef Google scholar
[26]
Nieves-Cordones M, Mohamed S, Tanoi K, Kobayashi NI, Takagi K, Vernet A et al (2017) Production of low-Cs+ rice plants by inactivation of the K+ transporter OsHAK1 with the CRISPR-Cas system. Plant J 92:43–56. https://doi.org/10.1111/tpj.13632
[27]
Nieves-Cordones M, Lara A, Ródenas R, Amo J, Rivero RM, Martínez V et al (2019) Modulation of K+ translocation by AKT1 and AtHAK5 in Arabidopsis plants. Plant Cell Environ 42:2357–2371. https://doi.org/10.1111/pce.13573
[28]
OhtaS, MitaS, HattoriT, NakamuraK. Construction and expression in tobacco of a β-glucuronidase (GUS) reporter gene containing an intron within the coding sequence. Plant Cell Physiol, 1990, 31: 805-813
CrossRef Google scholar
[29]
Osakabe Y, Arinaga N, Umezawa T, Katsura S, Nagamachi K, Tanaka H et al (2013) Osmotic stress responses and plant growth controlled by potassium transporters in Arabidopsis. Plant Cell 25:609–624. https://doi.org/10.1105/tpc.112.105700
[30]
Osmolovskaya N, Shumilina J, Bureiko K, Chantseva V, Bilova T, Kuchaeva L et al (2020) Ion homeostasis response to nutrient-deficiency stress in plants. cell growth 61. https://doi.org/10.5772/intechopen.89398https://www.intechopen.com/chapters/69690
[31]
PyoYJ, GierthM, SchroederJI, ChoMH. High-affinity K+ transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and post germination growth under low-potassium conditions. Plant Physiol, 2010, 153: 863-875 https://doi.org/pp.110.154369
CrossRef Google scholar
[32]
Qi Z, Hampton CR, Shin R, Barkla BJ, White PJ, Schachtman DP (2008) The high affinity K+ transporter AtHAK5 plays a physiological role in planta at very low K+ concentrations and provides a caesium uptake pathway in Arabidopsis. J Exp Bot 59:595–607. https://doi.org/10.1093/jxb/erm330
[33]
QuinteroFJ, BlattMR. A new family of K+ transporters from Arabidopsis that are conserved across phyla. FEBS Lett, 1997, 415: 206-211
CrossRef Google scholar
[34]
Ragel P, Ródenas R, García-Martín E, Andrés Z, Villalta I, Nieves-Cordones M et al (2015) CIPK23 regulates HAK5-mediated high-affinity K+ uptake in Arabidopsis roots. Plant Physiol 169:01401. https://doi.org/10.1104/pp.15.01401
[35]
Rai H, Yokoyama S, Satoh-Nagasawa N, Furukawa J, Nomi T, Ito Y et al (2017) Cesium uptake by rice roots largely depends upon a single gene, HAK1, which encodes a potassium transporter. Plant Cell Physiol 58:1486–1493. https://doi.org/10.1093/pcp/pcx094
[36]
RajappaS, KrishnamurthyP, KumarPP. Regulation of AtKUP2 expression by bHLH and WRKY transcription factors helps to confer increased salt tolerance to Arabidopsis thaliana plants. Front Plant Sci, 2020, 11: 1-16
CrossRef Google scholar
[37]
Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, Palme K et al (2013) Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol 197:1130–1141. https://doi.org/10.1111/nph.12092
[38]
RubioF, Nieves-CordonesM, AlemánF, MartínezV. Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the high-affinity range of concentrations. Physiol Plant, 2008, 134: 598-608
CrossRef Google scholar
[39]
RubioF, AlemánF, Nieves-CordonesM, MartínezV. Studies on Arabidopsis athak5, atakt1 double mutants disclose the range of concentrations at which AtHAK5, AtAKT1 and unknown systems mediate K+ uptake. Physiol Plant, 2010, 139: 220-228
CrossRef Google scholar
[40]
Saito S, Hamamoto S, Moriya K, Matsuura A, Sato Y, Muto J et al (2018) N-myristoylation and S-acylation are common modifications of Ca2+-regulated Arabidopsis kinases and are required for activation of the SLAC1 anion channel. New Phytol 218:1504–1521. https://doi.org/10.1111/nph.15053
[41]
Santa-maría GE, Rubio F, Dubcovsky J, Rodríguez-navarroa A (1997) The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9:2281–2289. https://doi.org/10.1105/tpc.9.12.2281
[42]
Santa-María GE, Oliferuk S, Moriconi JI (2018) KT-HAK-KUP transporters in major terrestrial photosynthetic organisms: a twenty years tale. J Plant Physiol 226:77–90. https://doi.org/10.1016/j.jplph.2018.04.008
[43]
Sanz-FernándezM, Rodríguez-GonzálezA, SandalioLM, Romero-PuertasMC. Role of potassium transporter KUP8 in plant responses to heavy metals. Physiol Plant, 2021, 173: 180-190
CrossRef Google scholar
[44]
Sato Y, Nanatani K, Hamamoto S, Shimizu M, Takahashi M, Tabuchi-Kobayashi M et al (2014) Defining membrane spanning domains and crucial membrane-localized acidic amino acid residues for K+ transport of a Kup/HAK/KT-type Escherichia coli potassium transporter. J Biochem 155:315–323. https://doi.org/10.1093/jb/mvu007
[45]
SchleyerM, BakkerEP. Nucleotide sequence and 3′-end deletion studies indicate that the K+- uptake protein kup from Escherichia coli is composed of a hydrophobic core linked to a large and partially essential hydrophilic C terminus. J Bacteriol, 1993, 175: 6925-6931
CrossRef Google scholar
[46]
SharmaT, DreyerI, RiedelsbergerJ. The role of K(+) channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana. Front Plant Sci, 2013, 4: 224
CrossRef Google scholar
[47]
Tanudjaja E, Hoshi N, Su YH, Hamamoto S, Uozumi N (2017) Kup-mediated Cs+ uptake and Kdp-driven K+ uptake coordinate to promote cell growth during excess Cs+ conditions in Escherichia coli. Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-02164-7
[48]
Tascón I, Sousa JS, Corey RA, Mills DJ, Griwatz D, Aumüller N et al (2020) Structural basis of proton-coupled potassium transport in the KUP family. Nat Commun 11:1–10. https://doi.org/10.1038/s41467-020-14441-7
[49]
Templalexis D, Tsitsekian D, Liu C, Daras G, Šimura J, Moschou P et al (2021) Potassium transporter TRH1/KUP4 contributes to distinct auxin-mediated root system architecture responses. Plant Physiol 188:1043–1060. https://doi.org/10.1093/plphys/kiab472
[50]
Tong Z, Gao Z, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10:1–13. https://doi.org/10.1186/1471-2199-10-71
[51]
TsujiiM, TanudjajaE, UozumiN. Diverse physiological functions of cation proton antiporters across bacteria and plant cells. Int J Mol Sci, 2020, 21: 1-14
CrossRef Google scholar
[52]
Uozumi N (2001) Escherichia coli as an expression system for K+ transport systems from plants. Am J Physiol Cell Physiol 281:C733–9. https://doi.org/10.1152/ajpcell.2001.281.3.c733
[53]
WangM, ZhengQ, ShenQ, GuoS. The critical role of potassium in plant stress response. Int J Mol Sci, 2013, 14: 7370-7390
CrossRef Google scholar
[54]
WhitePJ, BroadleyMR. Mechanisms of caesium uptake by plants. New Phytol, 2000, 147: 241-256
CrossRef Google scholar
[55]
Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L et al (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360. https://doi.org/10.1016/j.cell.2006.06.011
[56]
Zhang M, Huang P, Ji Y, Wang S, Wang SS, Li Z et al (2020) KUP9 maintains root meristem activity by regulating K + and auxin homeostasis in response to low K. EMBO Rep 21:1–20. https://doi.org/10.15252/embr.202050164

Accesses

Citations

Detail

Sections
Recommended

/