Integrated Analysis of Metabolome and Transcriptome Reveals Insights for Low Phosphorus Tolerance in Wheat Seedling

Low phosphorus (LP) stress leads to a significant reduction in wheat yield, primarily in the reduction of biomass, the number of tillers and spike grains, the delay in heading and flowering, and the inhibition of starch synthesis and grouting. However, the differences in regulatory pathway responses to low phosphorus stress among different wheat genotypes are still largely unknown. In this study, metabolome and transcriptome analyses of G28 (LP-tolerant) and L143 (LP-sensitive) wheat varieties after 72 h of normal phosphorus (CK) and LP stress were performed. A total of 181 and 163 differentially accumulated metabolites (DAMs) were detected for G28CK vs. G28LP and L143CK vs. L143LP, respectively. Notably, the expression of pilocarpine (C07474) in G28CK vs. G28LP was significantly downregulated 4.77-fold, while the expression of neochlorogenic acid (C17147) in L143CK vs. L143LP was significantly upregulated 2.34-fold. A total of 4023 differentially expressed genes (DEGs) were acquired between G28 and L143, of which 1120 DEGs were considered as the core DEGs of LP tolerance of wheat after LP treatment. The integration of metabolomics and transcriptomic data further revealed that the LP tolerance of wheat was closely related to 15 metabolites and 18 key genes in the sugar and amino acid metabolism pathway. The oxidative phosphorylation pathway was enriched to four ATPases, two cytochrome c reductase genes, and fumaric acid under LP treatment. Moreover, PHT1;1, TFs (ARFA, WRKY40, MYB4, MYB85), and IAA20 genes were related to the Pi starvation stress of wheat roots. Therefore, the differences in LP tolerance of different wheat varieties were related to energy metabolism, amino acid metabolism, phytohormones, and PHT proteins, and precisely regulated by the levels of various molecular pathways to adapt to Pi starvation stress. Taken together, this study may help to reveal the complex regulatory process of wheat adaptation to Pi starvation and provide new genetic clues for further study on improving plant Pi utilization efficiency.

[1]  C. Navarro,et al.  Arsenite provides a selective signal that coordinates arsenate uptake and detoxification through the regulation of PHR1 stability in Arabidopsis. , 2022, Molecular plant.

[2]  Junpu Liu,et al.  Transcriptomic and Metabolomic Analysis of the Effects of Exogenous Trehalose on Salt Tolerance in Watermelon (Citrullus lanatus) , 2022, Cells.

[3]  H. Chen,et al.  Abscisic acid facilitates phosphate acquisition through the transcription factor ABA INSENSITIVE5 in Arabidopsis. , 2022, The Plant journal : for cell and molecular biology.

[4]  Junna Liu,et al.  Transcriptome and Metabolome Analyses Revealed the Response Mechanism of Quinoa Seedlings to Different Phosphorus Stresses , 2022, International journal of molecular sciences.

[5]  Cuiyue Liang,et al.  Proteomic Analysis Dissects Molecular Mechanisms Underlying Plant Responses to Phosphorus Deficiency , 2022, Cells.

[6]  G. Bonanomi,et al.  Plant metabolomics in biotic and abiotic stress: a critical overview , 2021, Phytochemistry Reviews.

[7]  A. Nunes‐Nesi,et al.  The effect of silicon supply on photosynthesis and carbohydrate metabolism in two wheat (Triticum aestivum L.) cultivars contrasting in response to phosphorus nutrition. , 2021, Plant physiology and biochemistry : PPB.

[8]  C. Navarro,et al.  Arsenite Provides A Selective Signal that Coordinates Arsenate Uptake and Detoxificacion Involving Regulation of PHR1 Stability in Arabidopsis thaliana. , 2021, Molecular plant.

[9]  H. Xue,et al.  TaMADS2-3D, a MADS transcription factor gene, regulates phosphate starvation responses in plants , 2021 .

[10]  Jianfeng Wang,et al.  Epichloë gansuensis Increases the Tolerance of Achnatherum inebrians to Low-P Stress by Modulating Amino Acids Metabolism and Phosphorus Utilization Efficiency , 2021, Journal of fungi.

[11]  Huajun Wang,et al.  Dynamic Responses of Barley Root Succinyl-Proteome to Short-Term Phosphate Starvation and Recovery , 2021, Frontiers in Plant Science.

[12]  Muhammad Bilal Shakoor,et al.  Engineered biochars for recovering phosphate and ammonium from wastewater: A review. , 2021, The Science of the total environment.

[13]  W. Plaxton,et al.  Recent Insights into the Metabolic Adaptations of Phosphorus Deprived Plants. , 2020, Journal of experimental botany.

[14]  Nadia Bouain,et al.  Plant resilience to phosphate limitation: current knowledge and future challenges , 2020, Critical reviews in biotechnology.

[15]  C. Hao,et al.  The MYB transcription factor TaPHR3-A1 is involved in phosphate signaling and governs yield-related traits in bread wheat (Triticum aestivum L.). , 2020, Journal of experimental botany.

[16]  R. McIntosh,et al.  Breeding new cultivars for sustainable wheat production , 2019 .

[17]  F. Xie,et al.  Effect of biochar on grain yield and leaf photosynthetic physiology of soybean cultivars with different phosphorus efficiencies , 2019, Journal of Integrative Agriculture.

[18]  Juren Zhang,et al.  The bHLH family member ZmPTF1 regulates drought tolerance in maize by promoting root development and abscisic acid synthesis , 2019, Journal of experimental botany.

[19]  T. Chiou,et al.  Sensing and Signaling of Phosphate Starvation - from Local to Long Distance. , 2018, Plant & cell physiology.

[20]  Feng Ren,et al.  The ARF7 and ARF19 Transcription Factors Positively Regulate PHOSPHATE STARVATION RESPONSE1 in Arabidopsis Roots1 , 2018, Plant Physiology.

[21]  J. Postma,et al.  Ethylene modulates root cortical senescence in barley , 2018, Annals of botany.

[22]  K. Ljung,et al.  Author Correction: A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate , 2018, Nature Communications.

[23]  Huajun Wang,et al.  Molecular Mechanisms of Acclimatization to Phosphorus Starvation and Recovery Underlying Full-Length Transcriptome Profiling in Barley (Hordeum vulgare L.) , 2018, Front. Plant Sci..

[24]  A. Fernie,et al.  An In Vivo Perspective of the Role(s) of the Alternative Oxidase Pathway. , 2017, Trends in plant science.

[25]  V. Rubio,et al.  Novel signals in the regulation of Pi starvation responses in plants: facts and promises. , 2017, Current opinion in plant biology.

[26]  Hai Wang,et al.  Light and Ethylene Coordinately Regulate the Phosphate Starvation Response through Transcriptional Regulation of PHOSPHATE STARVATION RESPONSE1 , 2017, Plant Cell.

[27]  Costanza Emanueli,et al.  Transcriptional and Post-transcriptional Gene Regulation by Long Non-coding RNA , 2017, Genom. Proteom. Bioinform..

[28]  P. Jiang,et al.  Roles, Regulation, and Agricultural Application of Plant Phosphate Transporters , 2017, Front. Plant Sci..

[29]  Hua-gang Huang,et al.  Overexpression of the phosphate transporter gene OsPT8 improves the Pi and selenium contents in Nicotiana tabacum , 2017 .

[30]  Ping Wu,et al.  Phosphate starvation induced OsPHR4 mediates Pi-signaling and homeostasis in rice , 2016, Plant Molecular Biology.

[31]  Deyue Yu,et al.  Integrating QTL mapping and transcriptomics identifies candidate genes underlying QTLs associated with soybean tolerance to low-phosphorus stress , 2016, Plant Molecular Biology.

[32]  Haopeng Yu,et al.  The Molecular Mechanism of Ethylene-Mediated Root Hair Development Induced by Phosphate Starvation , 2016, PLoS genetics.

[33]  Wei Wu,et al.  Physiological and comparative proteome analyses reveal low-phosphate tolerance and enhanced photosynthesis in a maize mutant owing to reinforced inorganic phosphate recycling , 2016, BMC Plant Biology.

[34]  W. Schmidt,et al.  The regulation and plasticity of root hair patterning and morphogenesis , 2016, Development.

[35]  Wen‐Hao Zhang,et al.  OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice , 2015, Journal of experimental botany.

[36]  M. Iqbal,et al.  Metabolite Profiling of Low-P Tolerant and Low-P Sensitive Maize Genotypes under Phosphorus Starvation and Restoration Conditions , 2015, PloS one.

[37]  Ping Wu,et al.  Genetic manipulation of a high-affinity PHR1 target cis-element to improve phosphorous uptake in Oryza sativa L. , 2015, Plant Molecular Biology.

[38]  Caihuan Tian,et al.  Suppression of Photosynthetic Gene Expression in Roots Is Required for Sustained Root Growth under Phosphate Deficiency1[W][OPEN] , 2014, Plant Physiology.

[39]  J. Fisahn,et al.  Expression of Sucrose Transporter cDNAs Specifically in Companion Cells Enhances Phloem Loading and Long-Distance Transport of Sucrose but Leads to an Inhibition of Growth and the Perception of a Phosphate Limitation1[W][OPEN] , 2014, Plant Physiology.

[40]  Wei-Hua Wu,et al.  Arabidopsis WRKY45 Transcription Factor Activates PHOSPHATE TRANSPORTER1;1 Expression in Response to Phosphate Starvation1[W][OPEN] , 2014, Plant Physiology.

[41]  Hao Cheng,et al.  The Acid Phosphatase-Encoding Gene GmACP1 Contributes to Soybean Tolerance to Low-Phosphorus Stress , 2014, PLoS genetics.

[42]  G. Vanlerberghe,et al.  Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants , 2013, International journal of molecular sciences.

[43]  H. Bohnert,et al.  Regulation of miR399f Transcription by AtMYB2 Affects Phosphate Starvation Responses in Arabidopsis1[W] , 2012, Plant Physiology.

[44]  Z. Li,et al.  Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone , 2012, BMC Plant Biology.

[45]  Jun Feng Xiao,et al.  Metabolite identification and quantitation in LC-MS/MS-based metabolomics. , 2012, Trends in analytical chemistry : TRAC.

[46]  L. Nussaume,et al.  Root developmental adaptation to phosphate starvation: better safe than sorry. , 2011, Trends in plant science.

[47]  W. Plaxton,et al.  Metabolic Adaptations of Phosphate-Starved Plants1 , 2011, Plant Physiology.

[48]  J. Hammond,et al.  Sugar Signaling in Root Responses to Low Phosphorus Availability1 , 2011, Plant Physiology.

[49]  L. Herrera-Estrella,et al.  Global expression pattern comparison between low phosphorus insensitive 4 and WT Arabidopsis reveals an important role of reactive oxygen species and jasmonic acid in the root tip response to phosphate starvation , 2011, Plant signaling & behavior.

[50]  Mingguang Lei,et al.  Genetic and Genomic Evidence That Sucrose Is a Global Regulator of Plant Responses to Phosphate Starvation in Arabidopsis1[W][OA] , 2011, Plant Physiology.

[51]  R. Bock,et al.  ATP Synthase Repression in Tobacco Restricts Photosynthetic Electron Transport, CO2 Assimilation, and Plant Growth by Overacidification of the Thylakoid Lumen[OA] , 2011, Plant Cell.

[52]  Javier Paz-Ares,et al.  A Central Regulatory System Largely Controls Transcriptional Activation and Repression Responses to Phosphate Starvation in Arabidopsis , 2010, PLoS genetics.

[53]  Fusuo Zhang,et al.  Two strategies for achieving higher yield under phosphorus deficiency in winter wheat grown in field conditions , 2010 .

[54]  Wei-Hua Wu,et al.  The WRKY6 Transcription Factor Modulates PHOSPHATE1 Expression in Response to Low Pi Stress in Arabidopsis[W][OA] , 2009, The Plant Cell Online.

[55]  L. Herrera-Estrella,et al.  Phosphate Availability Alters Lateral Root Development in Arabidopsis by Modulating Auxin Sensitivity via a Mechanism Involving the TIR1 Auxin Receptor[C][W][OA] , 2008, The Plant Cell Online.

[56]  A. Karthikeyan,et al.  Phosphate starvation responses are mediated by sugar signaling in Arabidopsis , 2007, Planta.

[57]  Ping Wu,et al.  OsPTF1, a Novel Transcription Factor Involved in Tolerance to Phosphate Starvation in Rice1[w] , 2005, Plant Physiology.

[58]  C. Vance,et al.  Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin. , 2001, Plant physiology.

[59]  H. Shao,et al.  Biochar had effects on phosphorus sorption and desorption in three soils with differing acidity , 2014 .

[60]  J. Wiskich,et al.  Adenylate control of respiration in plants: the contribution of rotenone-insensitive electron transport to ADP-limited oxygen consumption by soybean mitochondria , 1990 .