HORMONES AND SHIFTING ECOLOGY THROUGHOUT PLANT DEVELOPMENT

Hormones modulate complex suites of ecologically relevant behaviors through interactive cascades of signal transduction; evolutionary changes in the function of a single hormone can result in multiple changes in plant traits. Sites of hormone action and tissue sensitivity change throughout plant ontogeny, as embryos, seedlings, and reproductively mature plants cope with shifting suites of environmental variables and resource availability. Phenotypic plasticity and correlations and trade-offs between life history traits (such as resource use efficiency and allocation to growth and differentiation of meristems) also change as plants age; hormonal changes are central to these shifts. I synthesize evidence from the molecular and physiology literature and present novel data on mangrove propagules, seedlings, saplings, and trees. Together, these data demonstrate that several ecologically important traits are hormonally mediated (both in the short term and over evolutionary time) in the diversification of plant lineages. I focus on two hormones with contrasting action: (1) abscisic acid (ABA), which regulates internal plant osmotic stability, membrane integrity, seed dormancy, and stomatal conductance; and (2) cytokinins (zeatin and allied adenine derivatives), which promote cell division, stimulate growth, delay leaf senescence, enhance the capacity of tissues to act as N sinks, and help to transduce signals of light and nutrient availability. ABA and cytokinin levels are correlated with patterns of osmotic tolerance, photosynthesis, growth, and leaf longevity, and their concentrations in specific tissues change throughout plant development. Ecologists and evolutionary biologists are in a strong position now to creatively comprehend, predict, and potentially engineer plant strategies and adaptive trade-offs over plant lifetimes in light of emerging knowledge of hormones.

[1]  G. Salmond,et al.  Conserved virulence factor regulation and secretion systems in bacterial pathogens of plants and animals , 2005, European Journal of Plant Pathology.

[2]  K. Hasenstein,et al.  Effects of Salinity on Endogenous Aba, Iaa, Ja, and Sa in Iris hexagona , 2001, Journal of Chemical Ecology.

[3]  Y. Kamiya,et al.  Effect of environment and gibberellins on the early growth and development of the red mangrove, Rhizophora mangle L. , 1996, Plant Growth Regulation.

[4]  J. Coleman,et al.  Evidence that abscisic acid does not regulate a centralized whole-plant response to low soil-resource availability , 1996, Oecologia.

[5]  A. I. Kuklin,et al.  Catecholamines in plants , 1995, Journal of Plant Growth Regulation.

[6]  J. Schultz,et al.  Reassessment of interaction between gut detergents and tannins in lepidoptera and significance for gypsy moth larvae , 1992, Journal of Chemical Ecology.

[7]  E. Weiler.  Radioimmunoassays for the differential and direct analysis of free and conjugated abscisic acid in plant extracts , 1980, Planta.

[8]  John H. Loughrin,et al.  Volicitin, An Elicitor of Maize Volatiles in Oral Secretion of Spodoptera Exigua: Isolation and Bioactivity , 2004, Journal of Chemical Ecology.

[9]  Peter McCourt,et al.  Hormone evolution: The key to signalling , 2003, Nature.

[10]  Ivo Feussner,et al.  The lipoxygenase pathway. , 2003, Annual review of plant biology.

[11]  J. Gatehouse.  Plant resistance towards insect herbivores: a dynamic interaction. , 2002, The New phytologist.

[12]  M. Parniske,et al.  Evolution of signal transduction in intracellular symbiosis. , 2002, Trends in plant science.

[13]  May R. Berenbaum,et al.  Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes , 2002, Nature.

[14]  M. Lerdau.  Plants Talk--But Can They Listen? , 2002, Science.

[15]  Martin Wikelski,et al.  The physiology/life-history nexus , 2002 .

[16]  A. Berna,et al.  Ring up the curtain on DING proteins , 2002, FEBS letters.

[17]  E. Blée,et al.  Impact of phyto-oxylipins in plant defense. , 2002, Trends in plant science.

[18]  J. Schultz.  Shared Signals and the Potential for Phylogenetic Espionage Between Plants and Animals1 , 2002, Integrative and comparative biology.

[19]  Lijun Liu,et al.  Abscisic acid and cytokinins in the root exudates and leaves and their relationship to senescence and remobilization of carbon reserves in rice subjected to water stress during grain filling , 2002, Planta.

[20]  W. Pierpoint.  Can aspirin help identify leaf proteins active in defence responses , 2002 .

[21]  O. Eriksson.  Ontogenetic niche shifts and their implications for recruitment in three clonal Vaccinium shrubs: Vaccinium myrtillus, Vaccinium vitis-idaea, and Vaccinium oxycoccos , 2002 .

[22]  S. Lindquist,et al.  Hsp90 as a capacitor of phenotypic variation , 2002, Nature.

[23]  D. Eamus,et al.  Seasonal patterns of xylem sap pH, xylem abscisic acid concentration, leaf water potential and stomatal conductance of six evergreen and deciduous Australian savanna tree species , 2002 .

[24]  H. Weber.  Fatty acid-derived signals in plants. , 2002, Trends in plant science.

[25]  J. Kieber,et al.  Cytokinin Signaling in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010444. , 2002, The Plant Cell Online.

[26]  D. Cipollini.  Does competition magnify the fitness costs of induced responses in Arabidopsis thaliana? A manipulative approach , 2002, Oecologia.

[27]  J. Murphy,et al.  Herbivory: Caterpillar saliva beats plant defences , 2002, Nature.

[28]  Jean Clobert,et al.  Hormones, developmental plasticity and adaptation , 2002 .

[29]  C. Fankhauser.  Light perception in plants: cytokinins and red light join forces to keep phytochrome B active. , 2002, Trends in plant science.

[30]  A. E. Valdés,et al.  Could plant hormones be the basis of maturation indices in Pinus radiata , 2002 .

[31]  W. J. Davies,et al.  ABA-based chemical signalling: the co-ordination of responses to stress in plants. , 2002, Plant, cell & environment.

[32]  Stuart A. Casson,et al.  Peptides: new signalling molecules in plants. , 2002, Trends in plant science.

[33]  F. J. Luque,et al.  Rational design of reversible acetylcholinesterase inhibitors. , 2002, Mini reviews in medicinal chemistry.

[34]  Akihiko Nakano,et al.  Involvement of the Vacuoles of the Endodermis in the Early Process of Shoot Gravitropism in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010216. , 2002, The Plant Cell Online.

[35]  I. Baldwin,et al.  Plant responses to insect herbivory: the emerging molecular analysis. , 2002, Annual review of plant biology.

[36]  P. Becraft.  First published online as a Review in Advance on June 26, 2002 RECEPTOR KINASE SIGNALING IN PLANT DEVELOPMENT , 2022 .

[37]  Z. Ye.  Vascular tissue differentiation and pattern formation in plants. , 2002, Annual review of plant biology.

[38]  Aaron M. Ellison,et al.  Macroecology of mangroves: large-scale patterns and processes in tropical coastal forests , 2002, Trees.

[39]  J. Schultz,et al.  Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus , 2002, Oecologia.

[40]  T. Mitchell-Olds.  Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution , 2001 .

[41]  J. Weyers,et al.  Plant Hormones and the Control of Physiological Processes , 2001 .

[42]  T. Bisseling,et al.  Peptide signaling in plants , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[43]  N. Hausmann,et al.  Population Differentiation for Abscisic Acid Responsiveness in Impatiens capensis (Balsaminaceae) , 2001, International Journal of Plant Sciences.

[44]  S. Shiu,et al.  Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[45]  G. N. Amzallag.  Developmental Changes in Effect of Cytokinin and Gibberellin on Shoot K+ and Na+ Accumulation in Salt-Treated Sorghum Plants , 2001 .

[46]  T. Pons,et al.  Acclimation of plants to light gradients in leaf canopies: evidence for a possible role for cytokinins transported in the transpiration stream. , 2001, Journal of experimental botany.

[47]  I. Baldwin,et al.  Competition mediates costs of jasmonate‐induced defences, nitrogen acquisition and transgenerational plasticity in Nicotiana attenuata , 2001 .

[48]  R. Karban,et al.  Jasmonate‐mediated induced plant resistance affects a community of herbivores , 2001 .

[49]  S. Gilbert.  Ecological developmental biology: developmental biology meets the real world. , 2001, Developmental biology.

[50]  C. Weinig,et al.  PHENOTYPIC PLASTICITY EARLY IN LIFE CONSTRAINS DEVELOPMENTAL RESPONSES LATER , 2001, Evolution; international journal of organic evolution.

[51]  David B. Clark,et al.  GETTING TO THE CANOPY: TREE HEIGHT GROWTH IN A NEOTROPICAL RAIN FOREST , 2001 .

[52]  S. Davies.  TREE MORTALITY AND GROWTH IN 11 SYMPATRIC MACARANGA SPECIES IN BORNEO , 2001 .

[53]  J. Weyers,et al.  Relative control potential of abscisic acid, carbon dioxide and light in responses of Phaseolus vulgaris stomata. , 2001, Physiologia plantarum.

[54]  I. Baldwin,et al.  Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. , 2001, Plant physiology.

[55]  L. Rahme,et al.  Common mechanisms for pathogens of plants and animals. , 2001, Annual review of phytopathology.

[56]  T. Mitchell-Olds,et al.  Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways , 2001, Planta.

[57]  D. Kaiser,et al.  Building a multicellular organism. , 2001, Annual review of genetics.

[58]  C. Rock,et al.  Tansley Review No. 120: Pathways to abscisic acid-regulated gene expression. , 2000, The New phytologist.

[59]  E. Farnsworth.  The Ecology and Physiology of Viviparous and Recalcitrant Seeds , 2000 .

[60]  J. van Ryn,et al.  COX-2 selectivity and inflammatory processes. , 2000, Current medicinal chemistry.

[61]  H. Harmens,et al.  Is Partitioning of Dry Weight and Leaf Area Within Dactylis glomerata Affected by N and CO2Enrichment , 2000 .

[62]  N. Blackstone.  Redox control and the evolution of multicellularity. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[63]  G. Felton,et al.  Trade-offs between pathogen and herbivore resistance. , 2000, Current opinion in plant biology.

[64]  J. J. Moreno.  Resveratrol modulates arachidonic acid release, prostaglandin synthesis, and 3T6 fibroblast growth. , 2000, The Journal of pharmacology and experimental therapeutics.

[65]  P. Reymond,et al.  Differential Gene Expression in Response to Mechanical Wounding and Insect Feeding in Arabidopsis , 2000, Plant Cell.

[66]  R. Amasino,et al.  Increased cytokinin levels in transgenic PSAG12–IPT tobacco plants have large direct and indirect effects on leaf senescence, photosynthesis and N partitioning , 2000 .

[67]  Martin J. Mueller,et al.  Formation of isoprostane F(2)-like compounds (phytoprostanes F(1)) from alpha-linolenic acid in plants. , 2000, Free radical biology & medicine.

[68]  F. Ausubel,et al.  Caenorhabditis elegans: a model genetic host to study Pseudomonas aeruginosa pathogenesis. , 2000, Current opinion in microbiology.

[69]  W. Boland,et al.  Gut Bacteria May Be Involved in Interactions between Plants, Herbivores and Their Predators: Microbial Biosynthesis of N-Acylglutamine Surfactants as Elicitors of Plant Volatiles , 2000, Biological chemistry.

[70]  J. Coleman,et al.  BIOMASS ALLOCATION IN PLANTS: ONTOGENY OR OPTIMALITY? A TEST ALONG THREE RESOURCE GRADIENTS , 1999 .

[71]  D. Stanley.  Eicosanoids in Invertebrate Signal Transduction Systems , 1999 .

[72]  Cynthia S. Jones.  An Essay on Juvenility, Phase Change, and Heteroblasty in Seed Plants , 1999, International Journal of Plant Sciences.

[73]  L. Endres,et al.  Alteration of Hormonal Levels in a Rootless Epiphytic Bromeliad in Different Phenological Phases , 1999, Journal of Plant Growth Regulation.

[74]  James H. Brown,et al.  Allometric scaling of production and life-history variation in vascular plants , 1999, Nature.

[75]  J. Schmitt,et al.  THE GENETIC ARCHITECTURE OF PLASTICITY TO DENSITY IN IMPATIENS CAPENSIS , 1999, Evolution; international journal of organic evolution.

[76]  J. Kieber,et al.  Molecular mechanisms of cytokinin action. , 1999, Current opinion in plant biology.

[77]  P. Reich,et al.  Generality of leaf trait relationships: a test across six biomes: Ecology , 1999 .

[78]  G. N. Amzallag.  Adaptive nature of the transition phases in development: the case of Sorghum bicolor , 1999 .

[79]  U. Bonas,et al.  The Xanthomonas Hrp type III system secretes proteins from plant and mammalian bacterial pathogens. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[80]  K. Raffa,et al.  Effects of elicitation treatment and genotypic variation on induced resistance in Populus: impacts on gypsy moth (Lepidoptera: Lymantriidae) development and feeding behavior , 1999, Oecologia.

[81]  T. Sachs.  ‘Node counting’: an internal control of balanced vegetative and reproductive development , 1999 .

[82]  E. Ketterson,et al.  Adaptation, Exaptation, and Constraint: A Hormonal Perspective , 1999, The American Naturalist.

[83]  A. Stoka,et al.  Phylogeny and evolution of chemical communication: an endocrine approach. , 1999, Journal of molecular endocrinology.

[84]  G. Coruzzi,et al.  Molecular evolution of glutamate receptors: a primitive signaling mechanism that existed before plants and animals diverged. , 1999, Molecular biology and evolution.

[85]  Peter McCourt,et al.  GENETIC ANALYSIS OF HORMONE SIGNALING. , 1999, Annual review of plant physiology and plant molecular biology.

[86]  A. K. Cowan,et al.  Regulation of abscisic acid metabolism: towards a metabolic basis for abscisic acid-cytokinin antagonism , 1999 .

[87]  David D. Ackerly,et al.  Significance of leaf longevity in plants , 1999 .

[88]  E. Coen,et al.  Separation of shoot and floral identity in Arabidopsis. , 1999, Development.

[89]  S. Sarker,et al.  Plant natural products as insect steroid receptor agonists and antagonists , 1999 .

[90]  R. Karban,et al.  PLANT PHASE CHANGE AND RESISTANCE TO HERBIVORY , 1999 .

[91]  P. Lin,et al.  Dynamics of element contents during the development of hypocotyles and leaves of certain mangrove species , 1999 .

[92]  B. Sinervo,et al.  MECHANISTIC AND SELECTIVE CAUSES OF LIFE HISTORY TRADE-OFFS AND PLASTICITY , 1998 .

[93]  J. Coleman,et al.  Effects of nitrogen fertilization on leaf chemistry and beetle feeding are mediated by leaf development , 1998 .

[94]  J. Ellis,et al.  Structure and function of proteins controlling strain-specific pathogen resistance in plants. , 1998, Current opinion in plant biology.

[95]  E. Farnsworth,et al.  Reductions in abscisic acid are linked with viviparous reproduction in mangroves. , 1998, American journal of botany.

[96]  J. Giraudat,et al.  ABSCISIC ACID SIGNAL TRANSDUCTION. , 1998, Annual review of plant physiology and plant molecular biology.

[97]  A. Theologis,et al.  Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[98]  R. B. Willis,et al.  FOLIAGE DAMAGE DOES NOT AFFECT WITHIN‐SEASON TRANSMISSION OF AN INSECT VIRUS , 1998 .

[99]  R. Emery,et al.  Branch development in Lupinus angustifolius L. II. Relationship with endogenous ABA, IAA and cytokinins in axillary and main stem buds , 1998 .

[100]  E. Haukioja,et al.  Intra-plant regulation of growth and plant-herbivore interactions , 1998 .

[101]  J. Barnes,et al.  Influence of plant age on ozone resistance in Plantago major , 1998 .

[102]  T. Whitham,et al.  THE DEVELOPMENTAL STREAM OF COTTONWOODS AFFECTS RAMET GROWTH AND RESISTANCE TO GALLING APHIDS , 1998 .

[103]  R. Dixon,et al.  Evidence for Chewing Insect-Specific Molecular Events Distinct from a General Wound Response in Leaves , 1997, Plant physiology.

[104]  S. Ryu,et al.  Inhibition of phospholipase D by lysophosphatidylethanolamine, a lipid-derived senescence retardant. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[105]  Plant mutants with altered responses to cytokinins , 1997 .

[106]  Martin J. Mueller.  Enzymes involved in jasmonic acid biosynthesis , 1997 .

[107]  T. Schmülling,et al.  Cytokinins as regulators of gene expression , 1997 .

[108]  M. Pigliucci,et al.  Ontogenetic phenotypic plasticity during the reproductive phase in Arabidopsis thaliana (Brassicaceae). , 1997, American journal of botany.

[109]  R. Creelman,et al.  BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS. , 1997, Annual review of plant physiology and plant molecular biology.

[110]  C. Vertucci,et al.  Presence of dehydrin-like proteins and levels of abscisic acid in recalcitrant (desiccation sensitive) seeds may be related to habitat , 1996, Seed Science Research.

[111]  G. Howe,et al.  Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[112]  T. Elmqvist,et al.  The evolution of vivipary in flowering plants , 1996 .

[113]  A. Ellison,et al.  SUN-SHADE ADAPTABILITY OF THE RED MANGROVE, RHIZOPHORA MANGLE (RHIZOPHORACEAE) : CHANGES THROUGH ONTOGENY AT SEVERAL LEVELS OF BIOLOGICAL ORGANIZATION , 1996 .

[114]  J. Ingram,et al.  THE MOLECULAR BASIS OF DEHYDRATION TOLERANCE IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[115]  A. Ellison,et al.  Spatial and temporal variability in growth of Rhizophora mangle saplings on coral cays: links with variation in insolation, herbivory, and local sedimentation rate , 1996 .

[116]  J. Romero,et al.  Allocation of biomass and mineral elements in Melilotus segetalis (annual sweetclover): effects of NaCl salinity and plant age. , 1996, The New phytologist.

[117]  D. Wheatley,et al.  Cell survival and multiplication. The overriding need for signals: from unicellular to multicellular systems. , 1996, FEMS microbiology letters.

[118]  L. Voesenek,et al.  Plants and Hormones: An ecophysiological view on timing and plasticity , 1996 .

[119]  W. Boland,et al.  Induction of volatile biosynthesis in the Lima bean (Phaseolus lunatus) by leucine‐ and isoleucine conjugates of 1‐oxo‐ and 1‐hydroxyindan‐4‐carboxylic acid: evidence for amino acid conjugates of jasmonic acid as intermediates in the octadecanoid signalling pathway , 1995, FEBS letters.

[120]  S. Snedaker,et al.  Salinity Responses in Two Populations of Viviparous Rhizophora mangle L. Seedlings , 1995 .

[121]  Detlef Weigel,et al.  A developmental switch sufficient for flower initiation in diverse plants , 1995, Nature.

[122]  G. Bernier,et al.  Abscisic acid antagonizes the effect of cytokinin on DNA-replication origins , 1995 .

[123]  R. Poethig,et al.  Gibberellins Promote Vegetative Phase Change and Reproductive Maturity in Maize , 1995, Plant physiology.

[124]  H. Gardner.  BIOLOGICAL ROLES AND BIOCHEMISTRY OF THE LIPOXYGENASE PATHWAY , 1993, HortScience.

[125]  S. Neidle,et al.  Rationally designed analogues of tamoxifen with improved calmodulin antagonism. , 1995, Journal of medicinal chemistry.

[126]  P. J. Davies.  Plant hormones : physiology, biochemistry and molecular biology , 1995 .

[127]  J. Coleman,et al.  Interpreting phenotypic variation in plants. , 1994, Trends in ecology & evolution.

[128]  F. Stuart Chapin,et al.  Evolution of Suites of Traits in Response to Environmental Stress , 1993, The American Naturalist.

[129]  J. Farrant,et al.  The role of plant growth regulators in the development and germination of the desiccation-sensitive (recalcitrant) seeds of Avicennia marina , 1993, Seed Science Research.

[130]  S. Hoffmann-Benning,et al.  On the role of abscisic Acid and gibberellin in the regulation of growth in rice. , 1992, Plant physiology.

[131]  H. Poorter,et al.  Growth and carbon economy of a fast- growing and a slow-growing grass species as dependent on ontogeny , 1992 .

[132]  J. Medford,et al.  Inhibition of lipoxygenase and prostaglandin endoperoxide synthase by anacardic acids. , 1991, Biochemical and Biophysical Research Communications - BBRC.

[133]  M. Feder,et al.  On the future of animal physiological ecology , 1991 .

[134]  F. Stuart Chapin,et al.  Integrated Responses of Plants to Stress , 1991 .

[135]  M. Kogan,et al.  Induced resistance in soybean to the Mexican bean beetle (Coleoptera: Coccinellidae): comparisons of inducing factors. , 1990 .

[136]  Poethig Rs,et al.  Phase change and the regulation of shoot morphogenesis in plants. , 1990 .

[137]  T. Flowers,et al.  Salt Tolerance in the Halophyte Suaeda maritima L.Dum.: Abscisic Acid Concentrations in Response to Constant and Altered Salinity , 1988 .

[138]  M. Ball.  Salinity tolerance in the mangroves Aegiceras corniculatum and Avicennia marina. I: Water use in relation to growth, carbon partitioning, and salt balance , 1988 .

[139]  R. Huffaker,et al.  Plant Senescence: Its Biochemistry and Physiology , 1987 .

[140]  R. Legge,et al.  THE ROLE OF FREE RADICALS IN SENESCENCE AND WOUNDING. , 1987, The New phytologist.

[141]  P. Tomlinson,et al.  The botany of mangroves , 1987 .

[142]  A. Trewavas.  Resource allocation under poor growth conditions. A major role for growth substances in developmental plasticity. , 1986, Symposia of the Society for Experimental Biology.

[143]  David F. Rhoades,et al.  Offensive-Defensive Interactions between Herbivores and Plants: Their Relevance in Herbivore Population Dynamics and Ecological Theory , 1985, The American Naturalist.

[144]  J. Schultz,et al.  Oak Leaf Quality Declines in Response to Defoliation by Gypsy Moth Larvae , 1982, Science.

[145]  A. Cole,et al.  CYTOKININ PRODUCTION BY ECTOMYCORRHIZAL FUNGI , 1982 .

[146]  D. Janzen,et al.  Herbivores: Their Interaction With Secondary Plant Metabolites , 1982 .

[147]  G. Evans,et al.  The quantitative analysis of plant growth , 1972 .