Phosphoproteomic analysis of lettuce (Lactuca sativa L.) reveals starch and sucrose metabolism functions during bolting induced by high temperature

High temperatures induce early bolting in lettuce (Lactuca sativa L.), which decreases both quality and production. However, knowledge of the molecular mechanism underlying high temperature promotes premature bolting is lacking. In this study, we compared lettuce during the bolting period induced by high temperatures (33/25 °C, day/night) to which raised under controlled temperatures (20/13 °C, day/night) using iTRAQ-based phosphoproteomic analysis. A total of 3,814 phosphorylation sites located on 1,766 phosphopeptides from 987 phosphoproteins were identified after high-temperature treatment,among which 217 phosphoproteins significantly changed their expression abundance (116 upregulated and 101 downregulated). Most phosphoproteins for which the abundance was altered were associated with the metabolic process, with the main molecular functions were catalytic activity and transporter activity. Regarding the functional pathway, starch and sucrose metabolism was the mainly enriched signaling pathways. Hence, high temperature influenced phosphoprotein activity, especially that associated with starch and sucrose metabolism. We suspected that the lettuce shorten its growth cycle and reduce vegetative growth owing to changes in the contents of starch and soluble sugar after high temperature stress, which then led to early bolting/flowering. These findings improve our understanding of the regulatory molecular mechanisms involved in lettuce bolting.

[1]  C. Xie,et al.  Identifying changes in the wheat kernel proteome under heat stress using iTRAQ , 2018, The Crop Journal.

[2]  Jian-ke Li,et al.  Quantitative Proteomics Analysis of Lettuce (Lactuca sativa L.) Reveals Molecular Basis-Associated Auxin and Photosynthesis with Bolting Induced by High Temperature , 2018, International journal of molecular sciences.

[3]  I. Ciereszko Regulatory roles of sugars in plant growth and development , 2018, Acta Societatis Botanicorum Poloniae.

[4]  Y. Ruan,et al.  Evolution of Sucrose Metabolism: The Dichotomy of Invertases and Beyond. , 2017, Trends in plant science.

[5]  A. Wingler Transitioning to the Next Phase: The Role of Sugar Signaling throughout the Plant Life Cycle[OPEN] , 2017, Plant Physiology.

[6]  M. Moshelion,et al.  Sugar and hexokinase suppress expression of PIP aquaporins and reduce leaf hydraulics that preserves leaf water potential , 2017, The Plant journal : for cell and molecular biology.

[7]  P. Seo,et al.  Arabidopsis TOR signaling is essential for sugar-regulated callus formation. , 2017, Journal of integrative plant biology.

[8]  Liping Wang,et al.  Low Night Temperature Affects the Phloem Ultrastructure of Lateral Branches and Raffinose Family Oligosaccharide (RFO) Accumulation in RFO-Transporting Plant Melon (Cucumismelo L.) during Fruit Expansion , 2016, PloS one.

[9]  H. Hirt,et al.  The Role of MAPK Modules and ABA during Abiotic Stress Signaling. , 2016, Trends in plant science.

[10]  E. Baena-González,et al.  The Arabidopsis SR45 Splicing Factor, a Negative Regulator of Sugar Signaling, Modulates SNF1-Related Protein Kinase 1 Stability , 2016, Plant Cell.

[11]  Kouhei Tsumoto,et al.  Quantitative phosphoproteomics-based molecular network description for high-resolution kinase-substrate interactome analysis , 2016, Bioinform..

[12]  M. Marquès-Bueno,et al.  The Protein Kinase CK2 Mediates Cross-Talk between Auxin- and Salicylic Acid-Signaling Pathways in the Regulation of PINOID Transcription , 2016, PloS one.

[13]  E. Huq,et al.  Arabidopsis casein kinase 2 α4 subunit regulates various developmental pathways in a functionally overlapping manner. , 2015, Plant science : an international journal of experimental plant biology.

[14]  Nan Li,et al.  Phosphoproteomic analysis of the response of maize leaves to drought, heat and their combination stress , 2015, Front. Plant Sci..

[15]  T. Mészáros,et al.  Activation of AtMPK9 through autophosphorylation that makes it independent of the canonical MAPK cascades. , 2015, The Biochemical journal.

[16]  H. Xue,et al.  Casein kinase 1 regulates ethylene synthesis by phosphorylating and promoting the turnover of ACS5. , 2014, Cell reports.

[17]  J. Richter,et al.  The CK1 Family: Contribution to Cellular Stress Response and Its Role in Carcinogenesis , 2014, Front. Oncol..

[18]  Synan F. AbuQamar,et al.  MAPK cascades and major abiotic stresses , 2014, Plant Cell Reports.

[19]  S. Smeekens,et al.  Sugar signals and the control of plant growth and development. , 2014, Journal of experimental botany.

[20]  K. Siddique,et al.  Heat-stress-induced reproductive failures in chickpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers. , 2013, Functional plant biology : FPB.

[21]  Lin Zhu,et al.  Functional Phosphoproteomic Analysis Reveals That a Serine-62-Phosphorylated Isoform of Ethylene Response Factor110 Is Involved in Arabidopsis Bolting1[C][W][OA] , 2012, Plant Physiology.

[22]  Gabino Sanchez-Perez,et al.  Metabolism control over growth: a case for trehalose-6-phosphate in plants. , 2012, Journal of experimental botany.

[23]  M. Schmid,et al.  Regulation of flowering time: all roads lead to Rome , 2011, Cellular and Molecular Life Sciences.

[24]  R. Amasino,et al.  The Timing of Flowering1 , 2010, Plant Physiology.

[25]  T. Toyomasu,et al.  The endogenous level of GA(1) is upregulated by high temperature during stem elongation in lettuce through LsGA3ox1 expression. , 2009, Journal of plant physiology.

[26]  Weikai Yan,et al.  Genotype by environment interactions of heat stress disorder resistance in crisphead lettuce. , 2009 .

[27]  L. Johnson The regulation of protein phosphorylation. , 2009, Biochemical Society transactions.

[28]  M. Larsen,et al.  Analytical strategies for phosphoproteomics , 2009, Expert review of neurotherapeutics.

[29]  J. Ariño,et al.  A role for protein kinase CK2 in plant development: evidence obtained using a dominant-negative mutant. , 2008, The Plant journal : for cell and molecular biology.

[30]  I. Henderson,et al.  Control of Arabidopsis flowering: the chill before the bloom , 2004, Development.

[31]  Caroline G. Bowsher,et al.  Protein Phosphorylation in Amyloplasts Regulates Starch Branching Enzyme Activity and Protein–Protein Interactions , 2004, The Plant Cell Online.

[32]  R. Dhindsa,et al.  In vivo and in vitro activation of temperature‐responsive plant map kinases , 2002, FEBS letters.

[33]  H. Pörtner,et al.  Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. , 2002, The Journal of experimental biology.

[34]  K. Shinozaki,et al.  Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. , 2000, The Plant journal : for cell and molecular biology.

[35]  Stitt,et al.  High-temperature perturbation of starch synthesis is attributable to inhibition of ADP-glucose pyrophosphorylase by decreased levels of glycerate-3-phosphate in growing potato tubers , 1998, Plant physiology.

[36]  P. Horton,et al.  Effect of High Temperature on Photosynthesis in Beans (I. Oxygen Evolution and Chlorophyll Fluorescence) , 1996, Plant physiology.

[37]  I. Raskin,et al.  Effect of submergence on translocation, starch content and amylolytic activity in deep-water rice , 1984, Planta.