Embryogenic Competence Acquisition in Sugar Cane Callus Is Associated with Differential H+-Pump Abundance and Activity.

Somatic embryogenesis is an important biological process in several plant species, including sugar cane. Proteomics approaches have shown that H+ pumps are differentially regulated during somatic embryogenesis; however, the relationship between H+ flux and embryogenic competence is still unclear. This work aimed to elucidate the association between extracellular H+ flux and somatic embryo maturation in sugar cane. We performed a microsomal proteomics analysis and analyzed changes in extracellular H+-flux and H+-pump (P-H+-ATPase, V-H+-ATPase, and H+-PPase) activity in embryogenic and non-embryogenic callus. A total of 657 proteins were identified, 16 of which were H+ pumps. We observed that P-H+-ATPase and H+-PPase were more abundant in embryogenic callus. Compared to non-embryogenic callus, embryogenic callus showed higher H+ influx, especially on maturation day 14, as well as higher H+-pump activity (mainly, P-H+-ATPase and H+-PPase activity). H+-PPase appears to be the major H+ pump in embryogenic callus during somatic embryo formation, functioning in both vacuole acidification and PPi homeostasis. These results provide evidence for an association between higher H+-pump protein abundance and, consequently, higher H+ flux and embryogenic competence acquisition in the callus of sugar cane, allowing for the optimization of the somatic embryo conversion process by modulating the activities of these H+ pumps.

[1]  Yun Liu,et al.  Corrigendum: miR156-SPL modules regulate induction of somatic embryogenesis in citrus callus , 2018, Journal of experimental botany.

[2]  C. Santa-Catarina,et al.  Insights from Proteomic Studies into Plant Somatic Embryogenesis , 2018, Proteomics.

[3]  S. Carpentier,et al.  Somatic Embryogenesis in Coffee: The Evolution of Biotechnology and the Integration of Omics Technologies Offer Great Opportunities , 2017, Front. Plant Sci..

[4]  Vijay Kumar,et al.  New insights into plant somatic embryogenesis: an epigenetic view , 2017, Acta Physiologiae Plantarum.

[5]  Huilong Zhang,et al.  Populus euphratica J3 mediates root K+/Na+ homeostasis by activating plasma membrane H+-ATPase in transgenic Arabidopsis under NaCl salinity , 2017, Plant Cell, Tissue and Organ Culture (PCTOC).

[6]  S. Tripathy,et al.  Scope of Genetic Transformation in Sugarcane-A Review , 2017 .

[7]  Arthur J. Ragauskas,et al.  A review of sugarcane bagasse for second‐generation bioethanol and biopower production , 2016 .

[8]  M. Maeshima,et al.  Lack of H+-pyrophosphatase Prompts Developmental Damage in Arabidopsis Leaves on Ammonia-Free Culture Medium , 2016, Front. Plant Sci..

[9]  Stefan Tenzer,et al.  Label-free quantification in ion mobility–enhanced data-independent acquisition proteomics , 2016, Nature Protocols.

[10]  Jen-Ping Chung,et al.  Acidogenic growth model of embryogenic cell suspension culture and qualitative mass production of somatic embryos from triploid bananas , 2016, Plant Cell, Tissue and Organ Culture (PCTOC).

[11]  José A. Dianes,et al.  2016 update of the PRIDE database and its related tools , 2015, Nucleic Acids Res..

[12]  V. Silveira,et al.  Label-Free Quantitative Proteomics of Embryogenic and Non-Embryogenic Callus during Sugarcane Somatic Embryogenesis , 2015, PloS one.

[13]  Qiang Xu,et al.  Genomewide analysis of small RNAs in nonembryogenic and embryogenic tissues of citrus: microRNA- and siRNA-mediated transcript cleavage involved in somatic embryogenesis. , 2015, Plant biotechnology journal.

[14]  K. Chowdhury,et al.  NMR-based metabolomics profile comparisons to distinguish between embryogenic and non-embryogenic callus tissue of sugarcane at the biochemical level , 2015, In Vitro Cellular & Developmental Biology - Plant.

[15]  M. S. Fernandes,et al.  Humic matter elicits proton and calcium fluxes and signaling dependent on Ca2+-dependent protein kinase (CDPK) at early stages of lateral plant root development , 2015, Chemical and Biological Technologies in Agriculture.

[16]  Karl H. Mühling,et al.  Leaf ion homeostasis and plasma membrane H(+)-ATPase activity in Vicia faba change after extra calcium and potassium supply under salinity. , 2014, Plant physiology and biochemistry : PPB.

[17]  A. Façanha,et al.  A vacuolar H(+)-pyrophosphatase differential activation and energy coupling integrate the responses of weeds and crops to drought stress. , 2014, Biochimica et biophysica acta.

[18]  Andrew R. Jones,et al.  ProteomeXchange provides globally co-ordinated proteomics data submission and dissemination , 2014, Nature Biotechnology.

[19]  Stefan Tenzer,et al.  Drift time-specific collision energies enable deep-coverage data-independent acquisition proteomics , 2013, Nature Methods.

[20]  Chao-jun Zhang,et al.  Transcriptome profiling reveals auxin and cytokinin regulating somatic embryogenesis in different sister lines of cotton cultivar CCRI24. , 2013, Journal of integrative plant biology.

[21]  V. Silveira,et al.  Morphological and polyamine content changes in embryogenic and non-embryogenic callus of sugarcane , 2013, Plant Cell, Tissue and Organ Culture (PCTOC).

[22]  V. Silveira,et al.  Polyamines affect the cellular growth and structure of pro-embryogenic masses in Araucaria angustifolia embryogenic cultures through the modulation of proton pump activities and endogenous levels of polyamines. , 2013, Physiologia plantarum.

[23]  S. Shabala,et al.  Haem oxygenase modifies salinity tolerance in Arabidopsis by controlling K+ retention via regulation of the plasma membrane H+-ATPase and by altering SOS1 transcript levels in roots , 2013, Journal of experimental botany.

[24]  P. Arruda.  Genetically modified sugarcane for bioenergy generation. , 2012, Current opinion in biotechnology.

[25]  S. Yuan,et al.  Effects of pH, MES, arabinogalactan-proteins on microspore cultures in white cabbage , 2012, Plant Cell, Tissue and Organ Culture (PCTOC).

[26]  R. Clayton,et al.  A computational model of auxin and pH dynamics in a single plant cell. , 2012, Journal of theoretical biology.

[27]  Jon K. Pittman,et al.  Multiple Transport Pathways for Mediating Intracellular pH Homeostasis: The Contribution of H+/ion Exchangers , 2012, Front. Plant Sci..

[28]  G. Horiguchi,et al.  Regulation of pyrophosphate levels by H+-PPase is central for proper resumption of early plant development , 2012, Plant signaling & behavior.

[29]  G. Horiguchi,et al.  Keep an Eye on PPi: The Vacuolar-Type H+-Pyrophosphatase Regulates Postgerminative Development in Arabidopsis[C][W][OA] , 2011, Plant Cell.

[30]  P. Arruda.  Perspective of the Sugarcane Industry in Brazil , 2011, Tropical Plant Biology.

[31]  Yong‐Bao Pan.  Databasing Molecular Identities of Sugarcane (Saccharum spp.) Clones Constructed with Microsatellite (SSR) DNA Markers , 2010 .

[32]  C. He,et al.  Direct somatic embryogenesis and shoot organogenesis from leaf explants of Primulina tabacum , 2010, Biologia Plantarum.

[33]  Douglas S. Domingues,et al.  The Biotechnology Roadmap for Sugarcane Improvement , 2010, Tropical Plant Biology.

[34]  F. Olivares,et al.  Nitric oxide mediates humic acids-induced root development and plasma membrane H+-ATPase activation , 2010, Planta.

[35]  K. Al-Rasheid,et al.  Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation , 2010, Proceedings of the National Academy of Sciences.

[36]  J. Feijó,et al.  Proton (H+) flux signature for the presymbiotic development of the arbuscular mycorrhizal fungi. , 2008, The New phytologist.

[37]  J. Rodríguez-León,et al.  Exclusion of a Proton ATPase from the Apical Membrane Is Associated with Cell Polarity and Tip Growth in Nicotiana tabacum Pollen Tubes[W] , 2008, The Plant Cell Online.

[38]  K. Schumacher,et al.  Plant proton pumps , 2007, FEBS letters.

[39]  Omid Karami,et al.  Effect of sucrose concentrations on somatic embryogenesis in carnation (Dianthus caryophyllus L.) , 2006 .

[40]  M. Maeshima,et al.  Vacuolar transporters and their essential role in plant metabolism. , 2006, Journal of experimental botany.

[41]  Jen-Ping Chung,et al.  Triploid banana cell growth phases and the correlation of medium pH changes with somatic embryogenesis in embryogenic cell suspension culture , 2006, Plant Cell, Tissue and Organ Culture.

[42]  A. Murphy,et al.  Arabidopsis H+-PPase AVP1 Regulates Auxin-Mediated Organ Development , 2005, Science.

[43]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[44]  D. Kramer,et al.  Regulating the proton budget of higher plant photosynthesis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[45]  P. M. Neumann,et al.  The Spatially Variable Inhibition by Water Deficit of Maize Root Growth Correlates with Altered Profiles of Proton Flux and Cell Wall pH1 , 2004, Plant Physiology.

[46]  H. V. Van Onckelen,et al.  The Role of Auxin, pH, and Stress in the Activation of Embryogenic Cell Division in Leaf Protoplast-Derived Cells of Alfalfa1 , 2002, Plant Physiology.

[47]  K. Dietz,et al.  Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. , 2001, Journal of experimental botany.

[48]  M. Oropeza,et al.  Proteins related with embryogenic potential in callus and cell suspensions of sugarcane (Saccharum sp.) , 2001, In Vitro Cellular & Developmental Biology - Plant.

[49]  F. Tremblay,et al.  The role of sucrose during maturation of black spruce (Picea mariana) and white spruce (Picea glauca) somatic embryos. , 2001, Physiologia plantarum.

[50]  D. Kramer,et al.  The proton to electron stoichiometry of steady-state photosynthesis in living plants: A proton-pumping Q cycle is continuously engaged. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[51]  M. Palmgren,et al.  Energization of Plant Cell Membranes by H+-Pumping ATPases: Regulation and Biosynthesis , 1999, Plant Cell.

[52]  J. Feijó,et al.  Growing Pollen Tubes Possess a Constitutive Alkaline Band in the Clear Zone and a Growth-dependent Acidic Tip , 1999, The Journal of cell biology.

[53]  A. Façanha,et al.  Reversibility of H+-ATPase and H+-Pyrophosphatase in Tonoplast Vesicles from Maize Coleoptiles and Seeds , 1998 .

[54]  M. Maeshima,et al.  Molecular cloning of vacuolar H(+)-pyrophosphatase and its developmental expression in growing hypocotyl of mung bean. , 1998, Plant physiology.

[55]  M. Palmgren,et al.  The 14-3-3 protein interacts directly with the C-terminal region of the plant plasma membrane H(+)-ATPase. , 1997, The Plant cell.

[56]  P. Thavarungkul.  Vibrating probe measurement of ionic currents around developing embryo of oil palm (Elaeis guineensis Jacq.) , 1997 .

[57]  M. Desbiez,et al.  Is cytoplasmic pH involved in the regulation of cell cycle in plants , 1994 .

[58]  J. Davies,et al.  Vacuolar H(+)-pumping ATPase variable transport coupling ratio controlled by pH. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[59]  D. P. Briskin,et al.  Proton Transport in Plasma Membrane and Tonoplast Vesicles from Red Beet (Beta vulgaris L.) Storage Tissue : A Comparative Study of Ion Effects on ΔpH and ΔΨ , 1987 .

[60]  R. Overall,et al.  Ionic currents traversing cell clusters from carrot suspension cultures reveal perpetuation of morphogenetic potential as distinct from induction of embryogenesis. , 1987, Cell differentiation.

[61]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[62]  R. Clárk.  Characterization of phosphatase of intact maize roots. , 1975, Journal of agricultural and food chemistry.

[63]  F. Skoog,et al.  A revised medium for rapid growth and bio assays with tobacco tissue cultures , 1962 .

[64]  C. Santa-Catarina,et al.  Putrescine induces somatic embryo development and proteomic changes in embryogenic callus of sugarcane. , 2016, Journal of proteomics.