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ZxSKOR is important for salinity and drought tolerance of Zygophyllum xanthoxylum by maintaining K+ homeostasis

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Abstract

As an important nutrient element, K+ plays a crucial role in plant stress resistance. It was reported that the stelar K+ outward rectifying channel (SKOR) is involved in loading K+ into xylem for its transport from roots to shoots. Zygophyllum xanthoxylum, a succulent woody xerophyte, could maintain stable K+ concentration in leaves to adapt to salt and arid environments. Here we characterized ZxSKOR from Z. xanthoxylum, ZxSKOR expression patterns and Na+ and K+ accumulation in Z. xanthoxylum treated with various concentrations of KCl and NaCl and −0.5 MPa osmotic stress were investigated in order to assess the contribution of ZxSKOR to K+ homeostasis. The results showed that ZxSKOR was predominantly expressed in roots and stems rather than in leaves. Its expression levels in roots and stems increased significantly accompanied by an increase in K+ concentration in leaves when plants were exposed to 5–10 mM KCl. Moreover, a positive correlation was identified not only between ZxSKOR expression in roots and K+ accumulation in shoots, but also between ZxSKOR expression in stems and K+ accumulation in leaves. Transcription levels of ZxSKOR in roots and stems under high salinity (100–150 mM NaCl) and osmotic stress (−0.5 MPa) were 2.0–2.8 times those in plants grown in the absence of NaCl or osmotic stress. Concomitantly, the expression level of ZxSKOR in roots under osmotic stress plus salt (−0.5 MPa +50 mM NaCl) was significantly higher than that under osmotic stress (−0.5 MPa) alone during 12–48 h of treatment. We propose that ZxSKOR in roots and stems is well-coordinated to mediate long-distance K+ transport and perhaps plays an important role in K+ accumulation and homeostasis in Z. xanthoxylum under salt as well as drought stress.

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Abbreviations

AKT:

Arabidopsis K+ transporter

ANOVA:

Analysis of variance

bp:

Base pair

FWC:

Field water capacity

GORK:

Guard rectifying K+ channel

HKT:

High affinity K+ transporter

KAT:

K+ Arabidopsis channel

KIRC:

K+ inward rectifying channel

KORC:

K+ outward rectifying channel

MPa:

Megapascal

NHX:

Tonoplast Na+/H+ antiporter

ORF:

Open reading frame

RT-PCR:

Reverse transcription polymerase chain reaction

SKOR:

Stelar K+ outward rectifying channel

SOS1:

Plasma membrane Na+/H+ antiporter

XPCs:

Xylem parenchyma cells

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Acknowledgments

We are very grateful to Professor Timothy J. Flowers from University of Sussex, UK, for critically reviewing the manuscript and for valuable suggestions. This work was supported by the National Basic Research Program of China (973 Program, Grant No. 2014CB138701), the National Natural Science Foundation of China (Grant Nos. 31222053, 31470503 and 31501994), the Specialized Research Fund for the Doctoral Program of Higher Education of China (Grant No. 20130211130001).

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Authors and Affiliations

  1. State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, 730020, People’s Republic of China

    Jing Hu, Qing Ma, Tanweer Kumar, Hui-Rong Duan, Jin-Lin Zhang, Hui-Jun Yuan, Qian Wang, Sardar Ali Khan, Pei Wang & Suo-Min Wang

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  1. Jing Hu
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  2. Qing Ma
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Correspondence to Suo-Min Wang.

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Supplementary Fig. S1

Zygophyllum xanthoxylum. The photographs (a, b) show the landscape, the natural habitat and the morphological peculiarities of Z. xanthoxylum. These wild Z. xanthoxylum plants grew in Alxa League (39°05′N, 105°34′E; elevation 1360 m) in the Inner-Mongolia Autonomous Region of China. The mean annual rainfall and temperature of the area are 60–150 mm and 8 °C, respectively, and the mean annual wind velocity 3.4 to 4.7 m s−1 (TIFF 8175 kb)

Supplementary Fig. S2

Phenotype of three-week-old Zygophyllum xanthoxylum seedlings. (a) Three-week-old Z. xanthoxylum seedlings were cultured in plastic containers (5 cm3; 2 seedlings/container) filled with sand and irrigated with modified Hoagland nutrient solution. (b) Root phenotype of three-week-old Z. xanthoxylum seedlings (TIFF 12453 kb)

Supplementary Fig. S3

Sequence alignment of ZxSKOR with SKOR from other higher plants. The multiple comparison was generated using DNAMAN program. The identical amino acid residues are indicated with black background. The six putative transmembrane regions (labeled as S1–S6), putative cyclic nucleotide binding domain and ankyrin domain are underlined respectively. A pore region (P) is boxed with a red line. The sources and GenBank accession numbers of SKOR are as follows: ZxSKOR (Zygophyllum xanthoxylum), AtSKOR (Arabidopsis thaliana, NP_186934.1), GmSKOR (Glycine max, XP_003544361.1) (TIFF 9856 kb)

Supplementary Fig. S4

Hydrophilic plot of ZxSKOR from Z. xanthoxylum. Hydrophobicity values were calculated using the program TMPRED available at http://www.ch.embnet.org/software/ TMPRED form.html. The numbers in the Fig. (1–6) indicate the structures of the predicted transmembrane segments of ZxSKOR. The horizontal axis indicates the amino acid residues, and the vertical axis indicates hydrophobicity values (TIFF 11841 kb)

Supplementary Fig. S5

Sequence alignment of the S5-P interdomain of ZxSKOR with Shaker-like K+ channels from higher plants. The multiple comparison was generated using DNAMAN program. The sources and GenBank accession numbers of SKOR are as follows: ZxSKOR (Zygophyllum xanthoxylum), AtSKOR (Arabidopsis thaliana, NP_186934.1), ZxAKT1 (Z. xanthoxylum, ACX37089.1), AtKAT1 (A. thaliana, At5g46240), AtKC1 (A. thaliana, At4g32650) (TIFF 8695 kb)

Supplementary Fig. S6

Time courses of (a) Na+ and (b) K+ concentration in Z. xanthoxylum shoots under different concentrations of NaCl. Three-week-old seedlings were transferred into modified Hoagland solution supplemented with 50 and 150 mM NaCl over a 144 h period. Two seedlings were pooled in each replicate (n = 10). Values are mean ± SE (n = 3) and bars indicate SE. Data from Wu et al. (2011) (TIFF 11257 kb)

Supplementary Table S1

Primer sequences used in this study. P1, P2, P3, P4, P5 and P6 were used for cloning of ZxSKOR, semi-quantitative RT-PCR was performed with the specific primers P7 and P8, A1 and A2 were the specific primers of ACTIN (DOCX 15 kb)

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Hu, J., Ma, Q., Kumar, T. et al. ZxSKOR is important for salinity and drought tolerance of Zygophyllum xanthoxylum by maintaining K+ homeostasis. Plant Growth Regul 80, 195–205 (2016). https://doi.org/10.1007/s10725-016-0157-z

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