Transcriptional and metabolic responses of apple to different potassium environments

Potassium (K) is one of the most important macronutrients for plant development and growth. The influence mechanism of different potassium stresses on the molecular regulation and metabolites of apple remains largely unknown. In this research, physiological, transcriptome, and metabolite analyses were compared under different K conditions in apple seedlings. The results showed that K deficiency and excess conditions influenced apple phenotypic characteristics, soil plant analytical development (SPAD) values, and photosynthesis. Hydrogen peroxide (H2O2) content, peroxidase (POD) activity, catalase (CAT) activity, abscisic acid (ABA) content, and indoleacetic acid (IAA) content were regulated by different K stresses. Transcriptome analysis indicated that there were 2,409 and 778 differentially expressed genes (DEGs) in apple leaves and roots under K deficiency conditions in addition to 1,393 and 1,205 DEGs in apple leaves and roots under potassium excess conditions, respectively. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment showed that the DEGs were involved in flavonoid biosynthesis, photosynthesis, and plant hormone signal transduction metabolite biosynthetic processes in response to different K conditions. There were 527 and 166 differential metabolites (DMAs) in leaves and roots under low-K stress as well as 228 and 150 DMAs in apple leaves and roots under high-K stress, respectively. Apple plants regulate carbon metabolism and the flavonoid pathway to respond to low-K and high-K stresses. This study provides a basis for understanding the metabolic processes underlying different K responses and provides a foundation to improve the utilization efficiency of K in apples.

[1]  Zhilan Ye,et al.  Comparative Analysis of Transcriptome Profiles Reveals the Mechanisms in the Difference of Low Potassium Tolerance among Cultivated and Tibetan Wild Barleys , 2022, Agronomy.

[2]  A. Parida,et al.  Potassium deficiency stress tolerance in peanut (Arachis hypogaea) through ion homeostasis, activation of antioxidant defense, and metabolic dynamics: Alleviatory role of silicon supplementation. , 2022, Plant physiology and biochemistry : PPB.

[3]  Zhengjun Qiu,et al.  Development of a low-cost portable device for pixel-wise leaf SPAD estimation and blade-level SPAD distribution visualization using color sensing , 2021, Comput. Electron. Agric..

[4]  Zhang Junke,et al.  Integrative physiological, transcriptome, and metabolome analysis reveals the effects of nitrogen sufficiency and deficiency conditions in apple leaves and roots , 2021, Environmental and Experimental Botany.

[5]  T. Ren,et al.  Potassium modulates central carbon metabolism to participate in regulating CO2 transport and assimilation in Brassica napus leaves. , 2021, Plant science : an international journal of experimental plant biology.

[6]  Guo-ping Zhang,et al.  Comprehensive dissection of primary metabolites in response to diverse abiotic stress in barley at seedling stage. , 2021, Plant physiology and biochemistry : PPB.

[7]  Wenbin Li,et al.  GmAKT1 is involved in K+ uptake and Na+/K+ homeostasis in Arabidopsis and soybean plants. , 2020, Plant science : an international journal of experimental plant biology.

[8]  K. Xiao,et al.  Multi-Omics Analyses Reveal the Molecular Mechanisms Underlying the Adaptation of Wheat (Triticum aestivum L.) to Potassium Deprivation , 2020, Frontiers in Plant Science.

[9]  W. Scheible,et al.  Transcriptional, metabolic, physiological and developmental responses of switchgrass to phosphorus limitation , 2020, Plant, cell & environment.

[10]  Y. Jiang,et al.  Effects of Potassium Levels on Plant Growth, Accumulation and Distribution of Carbon, and Nitrate Metabolism in Apple Dwarf Rootstock Seedlings , 2020, Frontiers in Plant Science.

[11]  A. Murphy,et al.  The Potassium Transporter OsHAK5 Alters Rice Architecture via ATP-Dependent Transmembrane Auxin Fluxes , 2020, Plant communications.

[12]  Peng Liu,et al.  Transcriptome analysis of maize seedling roots in response to nitrogen-, phosphorus-, and potassium deficiency , 2020, Plant and Soil.

[13]  P. Ahmad,et al.  Combined effects of brassinosteroid and kinetin mitigates salinity stress in tomato through the modulation of antioxidant and osmolyte metabolism. , 2019, Plant physiology and biochemistry : PPB.

[14]  Jian Shi,et al.  Identification of Potential Metabolites Mediating Bird's Selective Feeding on Prunus mira Flowers , 2019, BioMed research international.

[15]  Cuiyue Liang,et al.  Integration of metabolome and transcriptome analyses highlights soybean roots responding to phosphorus deficiency by modulating phosphorylated metabolite processes. , 2019, Plant physiology and biochemistry : PPB.

[16]  Wei-Hua Wu,et al.  ZmHAK5 and ZmHAK1 function in K+ uptake and distribution in maize under low K+ conditions. , 2019, Journal of integrative plant biology.

[17]  M. Frei,et al.  Potassium Ion Channel Gene OsAKT1 Affects Iron Translocation in Rice Plants Exposed to Iron Toxicity , 2019, Front. Plant Sci..

[18]  María López-Delacalle,et al.  Amelioration of the Oxidative Stress Generated by Simple or Combined Abiotic Stress through the K+ and Ca2+ Supplementation in Tomato Plants , 2019, Antioxidants.

[19]  Adam J. Carroll,et al.  Responses to K deficiency and waterlogging interact via respiratory and nitrogen metabolism. , 2019, Plant, cell & environment.

[20]  Z. Ren,et al.  Metabolite profiling and genome‐wide association studies reveal response mechanisms of phosphorus deficiency in maize seedling , 2019, The Plant journal : for cell and molecular biology.

[21]  P. Ahmad,et al.  Brassinosteroids Regulate Growth in Plants Under Stressful Environments and Crosstalk with Other Potential Phytohormones , 2018, Journal of Plant Growth Regulation.

[22]  L. Shi,et al.  Photosynthetic characteristics and metabolic analyses of two soybean genotypes revealed adaptive strategies to low-nitrogen stress. , 2018, Journal of plant physiology.

[23]  Guo-ping Zhang,et al.  Root and leaf metabolite profiles analysis reveals the adaptive strategies to low potassium stress in barley , 2018, BMC Plant Biology.

[24]  B. Jákli,et al.  Functioning of potassium and magnesium in photosynthesis, photosynthate translocation and photoprotection. , 2018, Physiologia plantarum.

[25]  Md. Anowar Hossain,et al.  Potassium: A Vital Regulator of Plant Responses and Tolerance to Abiotic Stresses , 2018 .

[26]  Jia Gu,et al.  fastp: an ultra-fast all-in-one FASTQ preprocessor , 2018, bioRxiv.

[27]  Jie Luo,et al.  Rewiring of the Fruit Metabolome in Tomato Breeding , 2018, Cell.

[28]  V. Gupta,et al.  Abiotic Stress Responses and Microbe-Mediated Mitigation in Plants: The Omics Strategies , 2017, Front. Plant Sci..

[29]  H. Krishnan,et al.  Metabolomic profiling from leaves and roots of tomato (Solanum lycopersicum L.) plants grown under nitrogen, phosphorus or potassium-deficient condition. , 2015, Plant science : an international journal of experimental plant biology.

[30]  Liming Lu,et al.  Transcriptome analysis reveals dynamic changes in the gene expression of tobacco seedlings under low potassium stress , 2015, Journal of Genetics.

[31]  Zhenghui Liu,et al.  Physiological response to potassium deficiency in three sweet potato (Ipomoea batatas [L.] Lam.) genotypes differing in potassium utilization efficiency , 2015, Acta Physiologiae Plantarum.

[32]  Zhenrui Huang,et al.  Transcriptome Profiling of Sugarcane Roots in Response to Low Potassium Stress , 2015, PloS one.

[33]  B. Mueller‐Roeber,et al.  Transcriptomic analysis of nitrogen starvation- and cultivar-specific leaf senescence in winter oilseed rape (Brassica napus L.). , 2015, Plant science : an international journal of experimental plant biology.

[34]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[35]  D. Huhman,et al.  Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation. , 2015, Plant, cell & environment.

[36]  Cuiying Li,et al.  Differences in the Efficiency of Potassium (K) Uptake and Use in Five Apple Rootstock Genotypes , 2014 .

[37]  Guo-ping Zhang,et al.  Comparative Transcriptome Profiling of Two Tibetan Wild Barley Genotypes in Responses to Low Potassium , 2014, PloS one.

[38]  C. Abdelly,et al.  Potassium deficiency in plants: effects and signaling cascades , 2014, Acta Physiologiae Plantarum.

[39]  L. Xiong,et al.  A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. , 2013, Molecular plant.

[40]  Wei-Hua Wu,et al.  Potassium transport and signaling in higher plants. , 2013, Annual review of plant biology.

[41]  A. Mustroph,et al.  Characterization of the Phosphofructokinase Gene Family in Rice and Its Expression Under Oxygen Deficiency Stress , 2013, Front. Plant Sci..

[42]  Jiang Tian,et al.  Proteomics dissection of plant responses to mineral nutrient deficiency , 2013, Proteomics.

[43]  F. Rubio,et al.  Potassium starvation induces oxidative stress in Solanum lycopersicum L. roots. , 2012, Journal of plant physiology.

[44]  Wei-Hua Wu,et al.  Transcriptome analysis of rice root responses to potassium deficiency , 2012, BMC Plant Biology.

[45]  D. Schachtman,et al.  The Arabidopsis AP2/ERF transcription factor RAP2.11 modulates plant response to low-potassium conditions. , 2012, Molecular plant.

[46]  M. Talón,et al.  HKT2;2/1, a K⁺-permeable transporter identified in a salt-tolerant rice cultivar through surveys of natural genetic polymorphism. , 2012, The Plant journal : for cell and molecular biology.

[47]  Rong Zhou,et al.  Transcript Profile of the Response of Two Soybean Genotypes to Potassium Deficiency , 2012, PloS one.

[48]  A. Eneji,et al.  Genotypic variations in photosynthetic and physiological adjustment to potassium deficiency in cotton (Gossypium hirsutum). , 2012, Journal of photochemistry and photobiology. B, Biology.

[49]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[50]  Robert D. Hall,et al.  Plant Metabolomics in a nutshell: Potential and Future Challenges , 2011 .

[51]  H. El-Shemy,et al.  Potassium deficiency affects water status and photosynthetic rate of the vegetative sink in green house tomato prior to its effects on source activity. , 2011, Plant science : an international journal of experimental plant biology.

[52]  M. Hajirezaei,et al.  Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency , 2011 .

[53]  J. Schroeder,et al.  High-Affinity K+ Transport in Arabidopsis: AtHAK5 and AKT1 Are Vital for Seedling Establishment and Postgermination Growth under Low-Potassium Conditions1[C][W][OA] , 2010, Plant Physiology.

[54]  C. Lillo,et al.  Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. , 2010, Phytochemistry.

[55]  J. González,et al.  Soluble sugars , 2009, Plant signaling & behavior.

[56]  M. Stitt,et al.  Multilevel Analysis of Primary Metabolism Provides New Insights into the Role of Potassium Nutrition for Glycolysis and Nitrogen Assimilation in Arabidopsis Roots1[W][OA] , 2009, Plant Physiology.

[57]  D. Schachtman,et al.  Ethylene Mediates Response and Tolerance to Potassium Deprivation in Arabidopsis[W] , 2009, The Plant Cell Online.

[58]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[59]  A. Amtmann,et al.  The effect of potassium nutrition on pest and disease resistance in plants. , 2008, Physiologia plantarum.

[60]  C. Danna,et al.  The Ionic Environment Controls the Contribution of the Barley HvHAK1 Transporter to Potassium Acquisition1[W][OA] , 2008, Plant Physiology.

[61]  N. Nguyen,et al.  Depression of sink activity precedes the inhibition of biomass production in tomato plants subjected to potassium deficiency stress. , 2007, Journal of experimental botany.

[62]  Hank C Wu,et al.  Phosphorus Stress in Common Bean: Root Transcript and Metabolic Responses1[W][OA] , 2007, Plant Physiology.

[63]  Wei-Hua Wu,et al.  A Protein Kinase, Interacting with Two Calcineurin B-like Proteins, Regulates K+ Transporter AKT1 in Arabidopsis , 2006, Cell.

[64]  E. Baena-González,et al.  Sugar sensing and signaling in plants: conserved and novel mechanisms. , 2006, Annual review of plant biology.

[65]  M. Grant,et al.  Plant responses to potassium deficiencies: a role for potassium transport proteins. , 2006, Journal of experimental botany.

[66]  J. Schroeder,et al.  The Potassium Transporter AtHAK5 Functions in K+ Deprivation-Induced High-Affinity K+ Uptake and AKT1 K+ Channel Contribution to K+ Uptake Kinetics in Arabidopsis Roots1[w] , 2005, Plant Physiology.

[67]  Rainer Breitling,et al.  The Potassium-Dependent Transcriptome of Arabidopsis Reveals a Prominent Role of Jasmonic Acid in Nutrient Signaling1[w] , 2004, Plant Physiology.

[68]  F. Carrari,et al.  Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. , 2004, Current opinion in plant biology.

[69]  Sung-ju Ahn,et al.  Expression of KT/KUP Genes in Arabidopsis and the Role of Root Hairs in K+ Uptake , 2004, Plant Physiology.

[70]  W. Weckwerth.  Metabolomics in systems biology. , 2003, Annual review of plant biology.

[71]  B. Cubero,et al.  Inventory and Functional Characterization of the HAK Potassium Transporters of Rice1 , 2002, Plant Physiology.

[72]  J. Schroeder,et al.  AtKUP1: An Arabidopsis Gene Encoding High-Affinity Potassium Transport Activity , 1998, Plant Cell.

[73]  F. Rubio,et al.  The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. , 1997, The Plant cell.

[74]  U. Nehls,et al.  Evidence for an up-regulation of the host and a down-regulation of the fungal phosphofructokinase activity in ectomycorrhizas of Norway spruce and fly agaric. , 1996, The New phytologist.

[75]  J. Ward,et al.  Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake. , 1994, Annual review of biophysics and biomolecular structure.

[76]  M. Tester,et al.  Direct measurement of k channels in thylakoid membranes by incorporation of vesicles into planar lipid bilayers. , 1989, Plant physiology.

[77]  D. R. Hoagland,et al.  The Water-Culture Method for Growing Plants Without Soil , 2018 .