Carbon Fluxes between Primary Metabolism and Phenolic Pathway in Plant Tissues under Stress

Higher plants synthesize an amazing diversity of phenolic secondary metabolites. Phenolics are defined secondary metabolites or natural products because, originally, they were considered not essential for plant growth and development. Plant phenolics, like other natural compounds, provide the plant with specific adaptations to changing environmental conditions and, therefore, they are essential for plant defense mechanisms. Plant defensive traits are costly for plants due to the energy drain from growth toward defensive metabolite production. Being limited with environmental resources, plants have to decide how allocate these resources to various competing functions. This decision brings about trade-offs, i.e., promoting some functions by neglecting others as an inverse relationship. Many studies have been carried out in order to link an evaluation of plant performance (in terms of growth rate) with levels of defense-related metabolites. Available results suggest that environmental stresses and stress-induced phenolics could be linked by a transduction pathway that involves: (i) the proline redox cycle; (ii) the stimulated oxidative pentose phosphate pathway; and, in turn, (iii) the reduced growth of plant tissues.

[1]  Camille Bénard,et al.  The 'trade-off' between synthesis of primary and secondary compounds in young tomato leaves is altered by nitrate nutrition: experimental evidence and model consistency. , 2009, Journal of experimental botany.

[2]  D. Treutter Significance of flavonoids in plant resistance: a review , 2006 .

[3]  I. Graham,et al.  The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues , 2001 .

[4]  L. Plas,et al.  Relation between primary and secondary metabolism in plant cell suspensions , 1995, Plant Cell, Tissue and Organ Culture.

[5]  S. Larsson,et al.  Testing the growth-differentiation balance hypothesis: dynamic responses of willows to nutrient availability. , 2007, The New phytologist.

[6]  P. Broun Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. , 2005, Current opinion in plant biology.

[7]  J. Salminen,et al.  Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance , 2010, Oecologia.

[8]  G. Liakopoulos,et al.  Boron deficiency and concentrations and composition of phenolic compounds in Olea europaea leaves: a combined growth chamber and field study. , 2005, Tree physiology.

[9]  C. Lütz Cell physiology of plants growing in cold environments , 2010, Protoplasma.

[10]  C Lehfeldt,et al.  Cloning of the SNG1 Gene of Arabidopsis Reveals a Role for a Serine Carboxypeptidase-like Protein as an Acyltransferase in Secondary Metabolism , 2000, Plant Cell.

[11]  G. Yelenosky,et al.  Evaluation of Polyamine and Proline Levels during Low Temperature Acclimation of Citrus. , 1987, Plant physiology.

[12]  R. Dixon,et al.  Stress-Induced Phenylpropanoid Metabolism. , 1995, The Plant cell.

[13]  S. Arpaia,et al.  Role of endogenous flavonoids in resistance mechanism of Vigna to aphids. , 2000, Journal of agricultural and food chemistry.

[14]  C. Dunand,et al.  Reactive oxygen species during plant-microorganism early interactions. , 2010, Journal of integrative plant biology.

[15]  J. Koricheva,et al.  Biosynthetic origin of carbon-based secondary compounds: cause of variable responses of woody plants to fertilization? , 1998, CHEMOECOLOGY.

[16]  N. Sreenivasulu,et al.  Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance , 2005 .

[17]  V. Rubio,et al.  A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. , 2001, Genes & development.

[18]  Christopher B. Field,et al.  Plant Responses to Multiple Environmental FactorsPhysiological ecology provides tools for studying how interacting environmental resources control plant growth , 1987 .

[19]  P. Urwin,et al.  The interaction of plant biotic and abiotic stresses: from genes to the field. , 2012, Journal of experimental botany.

[20]  D. Selmar,et al.  New insights explain that drought stress enhances the quality of spice and medicinal plants: potential applications , 2014, Agronomy for Sustainable Development.

[21]  P. D. Hare,et al.  Metabolic implications of stress-induced proline accumulation in plants , 1997, Plant Growth Regulation.

[22]  C. Ballaré,et al.  Remote sensing of future competitors: impacts on plant defenses. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Rebecca E. Irwin,et al.  Direct and ecological costs of resistance to herbivory , 2002 .

[24]  Peter G. Waterman,et al.  Phenolic Content of Vegetation in Two African Rain Forests: Ecological Implications , 1978, Science.

[25]  A. Polle,et al.  Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. , 2002, Journal of experimental botany.

[26]  B. Ncube,et al.  Dissecting the stress metabolic alterations in in vitro Cyrtanthus regenerants. , 2013, Plant physiology and biochemistry : PPB.

[27]  A. Boudet Evolution and current status of research in phenolic compounds. , 2007, Phytochemistry.

[28]  Response of barley seedlings to UV-B radiation as affected by NaCl. , 2003, Journal of plant physiology.

[29]  G. C. Yeh,et al.  Transfer of 1-pyrroline-5-carboxylate as oxidizing potential from hepatocytes to erythrocytes. , 1982, The Biochemical journal.

[30]  Kazuo Shinozaki,et al.  Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. , 2006, Annual review of plant biology.

[31]  M. Stitt,et al.  A Small Decrease of Plastid Transketolase Activity in Antisense Tobacco Transformants Has Dramatic Effects on Photosynthesis and Phenylpropanoid Metabolism , 2001, Plant Cell.

[32]  F. Breusegem,et al.  Opinion on the possible role of flavonoids as energy escape valves: novel tools for nature's Swiss army knife? , 2010 .

[33]  J. Bergelson,et al.  Costs of induced responses in plants , 2003 .

[34]  V. Lattanzio,et al.  Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. , 2013, Plant physiology and biochemistry : PPB.

[35]  M. Stitt,et al.  Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. , 2006, The Plant journal : for cell and molecular biology.

[36]  C. Poschenrieder,et al.  The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). , 2001, Journal of experimental botany.

[37]  Linda Chalker-Scott,et al.  Environmental Significance of Anthocyanins in Plant Stress Responses , 1999 .

[38]  M. Hirai,et al.  Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. , 2005, The Plant journal : for cell and molecular biology.

[39]  A. Boudet,et al.  Phenylpropanoid and anthocyanin changes in low-temperature treated winter oilseed rape leaves , 1999 .

[40]  D. Treutter Significance of Flavonoids in Plant Resistance and Enhancement of Their Biosynthesis , 2005, Plant biology.

[41]  K. Gould,et al.  Flavonoid functions in plants. , 2006 .

[42]  A. Cardinali,et al.  Browning phenomena in stored artichoke (Cynara scolymus L.) heads: enzymic or chemical reactions?. , 1994 .

[43]  I. Somssich,et al.  UV light selectively coinduces supply pathways from primary metabolism and flavonoid secondary product formation in parsley. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  N. Stamp Out Of The Quagmire Of Plant Defense Hypotheses , 2003, The Quarterly Review of Biology.

[45]  M. Simmonds Flavonoid-insect interactions: recent advances in our knowledge. , 2003, Phytochemistry.

[46]  V. Lattanzio,et al.  Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. , 2006 .

[47]  R. Bennett,et al.  Secondary metabolites in plant defence mechanisms. , 1994, The New phytologist.

[48]  C. B. Purrington Costs of resistance. , 2000, Current opinion in plant biology.

[49]  R. Dixon,et al.  Stress responses in alfalfa (Medicago sativa L.) XIX. Transcriptional activation of oxidative pentose phosphate pathway genes at the onset of the isoflavonoid phytoalexin response , 1995, Plant Molecular Biology.

[50]  N. Chiariello,et al.  Allocating Resources to Reproduction and DefenseNew assessments of the costs and benefits of allocation patterns in plants are relating ecological roles to resource use , 1987 .

[51]  K. Robards,et al.  Analytical chemistry of fruit bioflavonoids. A review. , 1997 .

[52]  Dorothee Staiger,et al.  Ultraviolet-B Radiation-Mediated Responses in Plants. Balancing Damage and Protection1 , 2003, Plant Physiology.

[53]  V. Lattanzio,et al.  Low temperature metabolism of apple phenolics and quiescence of Phlyctaena vagabunda. , 2001, Journal of agricultural and food chemistry.

[54]  James K. M. Brown Yield penalties of disease resistance in crops. , 2002, Current opinion in plant biology.

[55]  P. Kroon,et al.  Plant Phenolics – Secondary Metabolites with Diverse Functions , 2009 .

[56]  V. Walbot,et al.  Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: Enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings , 1994, Planta.

[57]  J. Salminen,et al.  Tree resistance to Lymantria dispar caterpillars: importance and limitations of foliar tannin composition , 2009, Oecologia.

[58]  R. Dietrich,et al.  Growth responses and fitness costs after induction of pathogen resistance depend on environmental conditions , 2005 .

[59]  Joseph P Noel,et al.  Structure-function relationships in plant phenylpropanoid biosynthesis. , 2005, Current opinion in plant biology.

[60]  M. Kuraś,et al.  Low temperature-induced modifications in cell ultrastructure and localization of phenolics in winter oilseed rape (Brassica napus L. var. oleifera L.) leaves. , 2002, Annals of botany.

[61]  V. Walbot,et al.  Gene Expression Profiling in Response to Ultraviolet Radiation in Maize Genotypes with Varying Flavonoid Content1[w] , 2003, Plant Physiology.

[62]  F. S. Chapin,et al.  The Mineral Nutrition of Wild Plants Revisited: A Re-evaluation of Processes and Patterns , 1999 .

[63]  Jian-Kang Zhu,et al.  Cell Signaling during Cold, Drought, and Salt Stress Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000596. , 2002, The Plant Cell Online.

[64]  May R. Berenbaum,et al.  Physiological price of an induced chemical defense: photosynthesis, respiration, biosynthesis, and growth , 1997, Oecologia.

[65]  J. Salminen,et al.  Hydrolyzable tannins as "quantitative defenses": limited impact against Lymantria dispar caterpillars on hybrid poplar. , 2009, Journal of insect physiology.

[66]  M. Reiss Plant resource allocation. , 1989, Trends in ecology & evolution.

[67]  J. Staden,et al.  Dissecting the roles of osmolyte accumulation during stress , 1998 .

[68]  P. A. Thompson Plant Phenolics , 1965, Nature.

[69]  H. Yoshioka,et al.  Elicitation of primary and secondary metabolism during defense in the potato , 2003, Journal of General Plant Pathology.

[70]  M. Schloter,et al.  Tuning growth versus defence–belowground interactions and plant resource allocation , 2009, Plant and Soil.

[71]  G. Samson,et al.  Causal relationship between growth inhibition, accumulation of phenolic metabolites, and changes of UV-induced fluorescences in nitrogen- deficient barley plants , 2004 .

[72]  C. Lillo,et al.  Differential expression of four Arabidopsis PAL genes; PAL1 and PAL2 have functional specialization in abiotic environmental-triggered flavonoid synthesis. , 2008, Journal of plant physiology.

[73]  A. Osbourn,et al.  Dissecting plant secondary metabolism - constitutive chemical defences in cereals. , 2003, The New phytologist.

[74]  A. Savouré,et al.  Proline: a multifunctional amino acid. , 2010, Trends in plant science.

[75]  Susan E. Hartley,et al.  A protein competition model of phenolic allocation , 1999 .

[76]  J. Briat,et al.  Cellular iron homeostasis and metabolism in plant , 2013, Front. Plant Sci..

[77]  David W. Lee,et al.  THE ORIGIN OF LAND PLANTS: A NEW LOOK AT AN OLD PROBLEM , 1980 .

[78]  V. Lattanzio,et al.  Relationship of secondary metabolism to growth in oregano (Origanum vulgare L.) shoot cultures under nutritional stress , 2009 .

[79]  D Scheel,et al.  Receptor-mediated activation of a MAP kinase in pathogen defense of plants. , 1997, Science.

[80]  V. Lattanzio Changes in phenolic compounds during the development and cold storage of artichoke (Cynara scolymus L.) heads , 1987 .

[81]  J. M. Palma,et al.  Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. , 2012, Plant, cell & environment.

[82]  V. Shulaev,et al.  Metabolomics for plant stress response. , 2008, Physiologia plantarum.

[83]  M Henry H Stevens,et al.  The growth-defense trade-off and habitat specialization by plants in Amazonian forests. , 2006, Ecology.

[84]  Kazuki Saito,et al.  Integrated metabolomics for abiotic stress responses in plants. , 2015, Current opinion in plant biology.

[85]  K. Shetty Role of proline-linked pentose phosphate pathway in biosynthesis of plant phenolics for functional food and environmental applications: a review , 2004 .

[86]  G. Y. You,et al.  The iron deficiency-induced phenolics secretion plays multiple important roles in plant iron acquisition underground , 2008, Plant signaling & behavior.

[87]  P. Coley,et al.  The resource availability hypothesis revisited: a meta‐analysis , 2011 .

[88]  B. Arnholdt‐Schmitt Stress-Induced Cell Reprogramming. A Role for Global Genome Regulation? , 2004, Plant Physiology.

[89]  J. Asta,et al.  Effect of solar radiation (UV and visible) at high altitude on CAM-cycling and phenolic compound biosynthesis in Sedum album , 1998 .

[90]  B. Logan,et al.  Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[91]  Jason G. Hamilton,et al.  The carbon–nutrient balance hypothesis: its rise and fall , 2001 .

[92]  Michael Fenner,et al.  Reproductive Allocation in Plants , 2012 .

[93]  E. Kruger,et al.  Competition- and resource-mediated tradeoffs between growth and defensive chemistry in trembling aspen (Populus tremuloides). , 2006, The New phytologist.

[94]  G. Y. You,et al.  Iron Deficiency-Induced Secretion of Phenolics Facilitates the Reutilization of Root Apoplastic Iron in Red Clover1 , 2007, Plant Physiology.

[95]  D. Selmar,et al.  Influencing the product quality by deliberately applying drought stress during the cultivation of medicinal plants , 2013 .

[96]  W. Kaiser,et al.  Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? , 2000 .

[97]  B. Usadel,et al.  Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. , 2007, Plant, cell & environment.

[98]  U. Margna,et al.  Different l-phenylalanine pools available for the biosynthesis of phenolics in buckwheat seedling tissues , 1989 .

[99]  Xiangdong Fu,et al.  Phosphate Starvation Root Architecture and Anthocyanin Accumulation Responses Are Modulated by the Gibberellin-DELLA Signaling Pathway in Arabidopsis1[OA] , 2007, Plant Physiology.

[100]  O. Fiehn Metabolomics – the link between genotypes and phenotypes , 2004, Plant Molecular Biology.

[101]  B. Klejdus,et al.  Phenylalanine ammonia-lyase activity and phenolic compounds accumulation in nitrogen-deficient Matricaria chamomilla leaf rosettes , 2007 .

[102]  J. Gershenzon,et al.  Constitutive plant toxins and their role in defense against herbivores and pathogens. , 2002, Current opinion in plant biology.

[103]  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.

[104]  Dieter Treutter,et al.  Effects of nitrogen supply on growth, contents of phenolic compounds and pathogen (scab) resistance of apple trees , 2005 .

[105]  A. Agrawal BENEFITS AND COSTS OF INDUCED PLANT DEFENSE FOR LEPIDIUM VIRGINICUM (BRASSICACEAE) , 2000 .

[106]  M. A. Kaplan,et al.  Phytochemical Evolution: The Redox Theory , 1993 .

[107]  A. Leyva,et al.  Low Temperature Induces the Accumulation of Phenylalanine Ammonia-Lyase and Chalcone Synthase mRNAs of Arabidopsis thaliana in a Light-Dependent Manner , 1995, Plant physiology.

[108]  K. Last,et al.  Clock Gene Evolution and Functional Divergence , 2004, Journal of biological rhythms.

[109]  Rainer Matyssek,et al.  Growth and Defence in Plants , 2012, Ecological Studies.

[110]  A. Fett-Neto,et al.  Plant secondary metabolism and challenges in modifying its operation: an overview. , 2010, Methods in molecular biology.

[111]  V. Lattanzio,et al.  Plant Phenolics: A Biochemical and Physiological Perspective , 2012 .

[112]  N. Lewis,et al.  Nitrogen recycling in phenylpropanoid metabolism , 1996 .

[113]  J. Richards,et al.  Trade-off between plant growth and defense? A comparison of sagebrush populations , 2002, Oecologia.

[114]  I. Somssich,et al.  Differential early activation of defense-related genes in elicitor-treated parsley cells , 1989, Plant Molecular Biology.

[115]  Facchini Plant secondary metabolism: out of the evolutionary abyss. , 1999, Trends in plant science.

[116]  S. Mehta,et al.  Heavy‐metal‐induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris , 1999 .

[117]  T. Swain Evolution of Flavonoid Compounds , 1975 .

[118]  E. Pichersky,et al.  Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. , 2000, Trends in plant science.

[119]  Kazuki Saito,et al.  Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids , 2013, The Plant journal : for cell and molecular biology.

[120]  J. Burdon,et al.  The fitness costs to plants of resistance to pathogens , 2003, Genome Biology.

[121]  D. Herms,et al.  The Dilemma of Plants: To Grow or Defend , 1992, The Quarterly Review of Biology.

[122]  F. Stuart Chapin,et al.  Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory , 1983 .

[123]  D. Cipollini STRETCHING THE LIMITS OF PLASTICITY: CAN A PLANT DEFEND AGAINST BOTH COMPETITORS AND HERBIVORES? , 2004 .

[124]  C. Pieterse,et al.  Costs and benefits of hormone-regulated plant defences , 2013 .

[125]  A. G. Briggs,et al.  Disruption of Poly(ADP-ribosyl)ation Mechanisms Alters Responses of Arabidopsis to Biotic Stress1[C][W][OA] , 2009, Plant Physiology.

[126]  C. Ballaré Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence. , 2009, Plant, cell & environment.

[127]  L. Graham,et al.  The origin of plants: body plan changes contributing to a major evolutionary radiation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[128]  Shuiqin Wu,et al.  Metabolic engineering of natural products in plants; tools of the trade and challenges for the future. , 2008, Current opinion in biotechnology.

[129]  D. Walters,et al.  Costs and trade-offs associated with induced resistance , 2007 .

[130]  G. Cooper-Driver,et al.  Role of Phenolics in Plant Evolution. , 1999 .

[131]  C. Ballaré,et al.  To grow or defend? Low red : far-red ratios reduce jasmonate sensitivity in Arabidopsis seedlings by promoting DELLA degradation and increasing JAZ10 stability. , 2014, The New phytologist.

[132]  G. Toth,et al.  Trade‐offs between phlorotannin production and annual growth in natural populations of the brown seaweed Ascophyllum nodosum , 1999 .

[133]  N. Lewis,et al.  Nitrogen Metabolism in Lignifying Pinus taeda Cell Cultures (*) , 1996, The Journal of Biological Chemistry.

[134]  Gokare A. Ravishankar,et al.  Influence of abiotic stress signals on secondary metabolites in plants , 2011, Plant signaling & behavior.

[135]  B. W. Shirley Flavonoids in seeds and grains: physiological function, agronomic importance and the genetics of biosynthesis , 1998, Seed Science Research.

[136]  O. Gottlieb Review article number 47 , 1989 .

[137]  S. Flint,et al.  Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with other climate change factors , 2007, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[138]  Mark Stitt,et al.  Genome-Wide Reprogramming of Primary and Secondary Metabolism, Protein Synthesis, Cellular Growth Processes, and the Regulatory Infrastructure of Arabidopsis in Response to Nitrogen1[w] , 2004, Plant Physiology.

[139]  Joseph P Noel,et al.  The chalcone synthase superfamily of type III polyketide synthases. , 2003, Natural product reports.

[140]  M. Wink Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores , 2004, Theoretical and Applied Genetics.

[141]  Marcel A K Jansen,et al.  Arabidopsis thaliana plants acclimated to low dose rates of ultraviolet B radiation show specific changes in morphology and gene expression in the absence of stress symptoms. , 2007, The New phytologist.

[142]  Proline and its metabolism enzymes in cucumber cell cultures during acclimation to salinity , 2013, Protoplasma.

[143]  James K. M. Brown A cost of disease resistance: paradigm or peculiarity? , 2003, Trends in genetics : TIG.

[144]  U. Margna Control at the level of substrate supply—an alternative in the regulation of phenylpropanoid accumulation in plant cells , 1977 .

[145]  Michael Wink,et al.  Biochemistry of plant secondary metabolism. , 2010 .

[146]  H. Lischke,et al.  Cost of resistance and tolerance under competition: the defense-stress benefit hypothesis , 2003, Evolutionary Ecology.

[147]  M. Oh,et al.  Secondary metabolism and antioxidants are involved in environmental adaptation and stress tolerance in lettuce. , 2009, Journal of plant physiology.

[148]  J. Grace,et al.  Plant resource allocation , 1998 .

[149]  E. Priesack,et al.  The plant's capacity in regulating resource demand. , 2005, Plant biology.

[150]  I. Somssich,et al.  Arabidopsis thaliana defense-related protein ELI3 is an aromatic alcohol:NADP+ oxidoreductase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[151]  M. Wink Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. , 2003, Phytochemistry.

[152]  O. Blokhina,et al.  Antioxidants, oxidative damage and oxygen deprivation stress: a review. , 2003, Annals of botany.

[153]  C. Stewart Inhibition of proline oxidation by water stress. , 1977, Plant physiology.

[154]  L. Björn,et al.  Terrestrial ecosystems, increased solar ultraviolet radiation and interactions with other climatic change factors. , 2003, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[155]  O. Zakhleniuk,et al.  Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. , 2004, Journal of experimental botany.

[156]  I. Somssich,et al.  Pathogen defence in plants — a paradigm of biological complexity , 1998 .

[157]  P. Hasegawa,et al.  Moderately increased constitutive proline does not alter osmotic stress tolerance , 1997 .

[158]  C. Hertweck,et al.  The biosynthetic logic of polyketide diversity. , 2009, Angewandte Chemie.

[159]  K. Yamaguchi-Shinozaki,et al.  A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. , 1996, The Plant cell.

[160]  I. Baldwin,et al.  Fitness costs of induced resistance: emerging experimental support for a slippery concept. , 2002, Trends in plant science.

[161]  V. Lattanzio Phenolic Compounds: Introduction 50 , 2013 .

[162]  Geza Hrazdina,et al.  Spatial Organization of Enzymes in Plant Metabolic Pathways , 1992 .

[163]  B. Winkel-Shirley,et al.  Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. , 2001, Plant physiology.

[164]  Gert B. Eijkel,et al.  Differences in relative growth rate in 11 grasses correlate with differences in chemical composition as determined by pyrolysis mass spectrometry , 1992, Oecologia.

[165]  R. M. Rivero,et al.  Abiotic and biotic stress combinations. , 2014, The New phytologist.

[166]  R. Mittler,et al.  Reactive oxygen gene network of plants. , 2004, Trends in plant science.

[167]  F. Stuart Chapin,et al.  Resource Availability and Plant Antiherbivore Defense , 1985, Science.

[168]  P. Ruoff,et al.  Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. , 2008, Plant, cell & environment.

[169]  J. Christie,et al.  Distinct UV-B and UV-A/blue light signal transduction pathways induce chalcone synthase gene expression in Arabidopsis cells. , 1996, The Plant cell.

[170]  C. P. Constabel,et al.  Defensive Roles of Polyphenol Oxidase in Plants , 2008 .

[171]  C. Ballaré,et al.  Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. , 2000, Plant physiology.

[172]  H. Poorter,et al.  Chemical composition of 24 wild species differing in relative growth rate , 1992 .

[173]  R. Gallagher Seeds: the ecology of regeneration in plant communities. , 2014 .

[174]  Robert D Hall,et al.  Plant molecular stress responses face climate change. , 2010, Trends in plant science.

[175]  Nicholas Smirnoff,et al.  The role of active oxygen in the response of plants to water deficit and desiccation. , 1993, The New phytologist.

[176]  J. Schmid,et al.  Molecular organization of the shikimate pathway in higher plants , 1995 .

[177]  M. Simmonds Importance of flavonoids in insect--plant interactions: feeding and oviposition. , 2001, Phytochemistry.

[178]  J. Salminen,et al.  Oxidation of Ingested Phenolics in the Tree-Feeding Caterpillar Orgyia leucostigma Depends on Foliar Chemical Composition , 2008, Journal of Chemical Ecology.

[179]  K. Robards Analytical chemistry of fruit bioflavonoids , 1997 .

[180]  Martin Müller,et al.  ADP-Glucose Pyrophosphorylase-Deficient Pea Embryos Reveal Specific Transcriptional and Metabolic Changes of Carbon-Nitrogen Metabolism and Stress Responses1[W] , 2008, Plant Physiology.

[181]  P. Hare Review article. Proline synthesis and degradation: a model system for elucidating stress-related signal transduction , 1999 .