The evolution of plant secretory structures and emergence of terpenoid chemical diversity

Annual Review of Plant Biology

Volumn 66, Issue , 2015, Pages 139-159

  Lange, Bernd Markus ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Fossil record; Glandular trichome; Resin duct; Secretory cavity

Indexed keywords

MARCHANTIOPHYTA; TRACHEOPHYTA;

TERPENE;

DISEASE RESISTANCE; EVOLUTION; HERBIVORY; METABOLISM; PLANT; PLANT DISEASE; PLANT STRUCTURES; TRICHOME;

BIOLOGICAL EVOLUTION; DISEASE RESISTANCE; HERBIVORY; PLANT DISEASES; PLANT STRUCTURES; PLANTS; TERPENES; TRICHOMES;

EID: 84928882522     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-043014-114639     Document Type: Article

References (100)

1. Agrawal AA. 2005. Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evol. Ecol. Res. 7:651-67
2. Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S. 2012. Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol. 194:28-45
3. Anterola A, Shanle E, Mansouri K, Schuette S, Renzaglia K. 2009. Gibberellin precursor is involved in spore germination in the moss Physcomitrella patens. Planta 229:1003-7
4. Asakawa Y, Ludwiczuk A, Nagashima F. 2013. Chemical constituents of Anthocerotophyta. In Chemical Constituents of Bryophytes: Bio-and Chemical Diversity, Biological Activity, and Chemosystematics, pp. 607-17. Prog. Chem. Org. Nat. Prod. Vol. 95. Vienna: Springer
5. Asakawa Y, Ludwiczuk A, Nagashima F. 2013. Chemical constituents of Bryophyta. In Chemical Constituents of Bryophytes: Bio-and Chemical Diversity, Biological Activity, and Chemosystematics, pp. 563-605. Prog. Chem. Org. Nat. Prod. Vol. 95. Vienna: Springer
6. Asakawa Y, Ludwiczuk A, Nagashima F. 2013. Chemical constituents of Marchantiophyta. In Chemical Constituents of Bryophytes: Bio-and Chemical Diversity, Biological Activity, and Chemosystematics, pp. 25-561. Prog. Chem. Org. Nat. Prod. Vol. 95. Vienna: Springer
7. Behnke HD, Herrmann S. 1978. Fine structure and development of laticifers in Gnetum gnemon L. Protoplasma 94:371-84
8. Blomquist GJ, Figueroa-Teran R, Aw M, Song M, Gorzalski A, et al. 2010. Pheromone production in bark beetles. Insect Biochem. Mol. Biol. 40:699-712
9. BoschM,Wright LP, Gershenzon J, Wasternack C, Hause B, et al. 2014. Jasmonic acid and its precursor 12-oxophytodienoic acid control different aspects of constitutive and induced herbivore defenses in tomato. Plant Physiol. 166:396-410
10. Boughton AJ, Hoover K, Felton GW. 2005. Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J. Chem. Ecol. 31:2211-16
11. Bowman JL. 2013. Walkabout on the long branches of plant evolution. Curr. Opin. Plant Biol. 16:70-77
12. Bray PS, Anderson KB. 2009. Identification of Carboniferous (320 million years old) class Ic amber. Science 326:132-34
13. Call V, Dilcher D. 1997. The fossil record of Eucommia (Eucommiaceae) in North America. Am. J. Bot. 84:798
14. Calvin M. 1980. Hydrocarbons from plants: analytical methods and observations. Naturwissenschaften 67:525-33
15. Cardé JP. 1984. Leucoplasts: A distinct kind of organelles lacking typical 70S ribosomes and free thylakoids. Eur. J. Cell Biol. 34:18-26
16. Carpenter KJ. 2006. Specialized structures in the leaf epidermis of basal angiosperms: morphology, distribution, and homology. Am. J. Bot. 93:665-81
17. Charon J, Launay J, Cardé JP. 1985. Spatial organization and volume density of leucoplasts in pine secretory cells. Protoplasma 138:45-53
18. Chen F, Tholl D, Bohlmann J, Pichersky E. 2011. The family of terpene synthases in plants: A mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J. 66:212-29
19. Cheng A, Wang L, Sun Y, Lou H. 2012. Identification and expression analysis of key enzymes of the terpenoids biosynthesis pathway of a liverwort Plagiochasma appendiculatum by EST analysis. Acta Physiol. Plant. 35:107-18
20. Cheniclet C, Cardé JP. 1985. Presence of leucoplasts in secretory cells and of monoterpenes in the essential oil: A correlative study. Israel J. Bot. 34:219-38
21. Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, et al. 2012. Origin of strigolactones in the green lineage. New Phytol. 195:857-71
22. Delwiche CF, Graham LE, ThomsonN. 1989. Lignin-like compounds and sporopollenin in Coleochaete, an algal model for land plant ancestry. Science 245:399-401
23. Dussourd DE, Hoyle AM. 2000. Poisoned plusiines: toxicity of milkweed latex and cardenolides to some generalist caterpillars. Chemoecology 10:11-16
24. Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, et al. 2012. Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat. Geosci. 5:459-62
25. Everaerts C, Grégoire JC, Merlin J. 1988. The toxicity of Norway spruce monoterpenes to two bark beetle species and their associates. In Mechanisms of Woody Plant Defenses Against Insects, ed. WJ Mattson, J Levieux, C Bernard-Dagan, pp. 335-44. New York: Springer
26. Fahn A. 1988. Secretory tissues in vascular plants. New Phytol. 108:229-57
27. Farrell BD, Dussourd DE, Mitter C. 1991. Escalation of plant defense: Do latex and resin canals spur plant diversification? Am. Nat. 138:881-900
28. Foster AS Gifford EM. 1974. Comparative Morphology of Vascular Plants. San Francisco: Freeman
29. Glas JJ, Schimmel BC, Alba JM, Escobar-Bravo R, Schuurink RC, Kant MR. 2012. Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int. J. Mol. Sci. 13:17077-103
30. Goiris K, Muylaert K, Voorspoels S, Noten B, De Paepe D, et al. 2014. Detection of flavonoids in microalgae from different evolutionary lineages. J. Phycol. 50:483-92
31. Graham LE, Gray J. 2001. The origin, morphology, and ecophysiology of early embryophytes: neontological and paleontological perspectives. In Plants Invade the Land: Evolutionary and Environmental Perspectives, ed. PG Gensel, D Edwards, pp. 140-58. New York: Columbia Univ. Press
32. Graham LE, Lewis LA, Taylor W, Wellman C, Cook M. 2014. Early terrestrialization: transition from algal to bryophyte grade. In Photosynthesis in Bryophytes and Early Land Plants, ed. DT Hanson, SK Rice, pp. 9-28. Adv. Photosynth. Respir. Vol. 37. Amsterdam: Springer
33. Hagel JM, Yeung EC, Facchini PJ. 2008. Got milk The secret life of laticifers. Trends Plant Sci. 13:631-39
34. Hayashi K, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S, et al. 2010. Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant Physiol. 153:1085-97
35. Hayashi K, Kawaide H, Notomi M, Sakigi Y, Matsuo A, Nozaki H. 2006. Identification and functional analysis of bifunctional ent-kaurene synthase from themoss Physcomitrella patens. FEBS Lett. 580:6175-81
36. He X, Sun Y, Zhu RL. 2013. The oil bodies of liverworts: unique and important organelles in land plants. Crit. Rev. Plant Sci. 32:293-302
37. Hemmerlin A, Harwood JL, Bach TJ. 2012. A raison d'etre for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog. Lipid Res. 51:95-148
38. HeneryML,Wallis IR, Stone C, FoleyWJ. 2008. Methyl jasmonate does not induce changes in Eucalyptus grandis leaves that alter the effect of constitutive defense on larvae of a specialist herbivore. Oecologia 156:847-59
39. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, et al. 2007. The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens. Plant Cell 19:3058-79
40. Hori K, Maruyama F, Fujisawa T, TogashiT, YamamotoN, et al. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5:3978
41. Hudgins JW, Christiansen E, Franceschi VR. 2003. Methyl jasmonate induces changes mimicking anatomical defenses in diverse members of the Pinaceae. Tree Physiol. 23:361-71
42. Hudgins JW, Christiansen E, Franceschi VR. 2004. Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: A phylogenetic perspective. Tree Physiol. 24:251-64
43. Ishida T, Kurata T, Okada K, Wada T. 2008. A genetic regulatory network in the development of trichomes and root hairs. Annu. Rev. Plant Biol. 59:365-86
44. Keeling CI, Bohlmann J. 2006. Diterpene resin acids in conifers. Phytochemistry 67:2415-23
45. Keene CK, Wagner GJ. 1985. Direct demonstration of duvatrienediol biosynthesis in glandular heads of tobacco trichomes. Plant Physiol. 79:1026-32
46. Konno K. 2011. Plant latex and other exudates as plant defense systems: roles of various defense chemicals and proteins contained therein. Phytochemistry 72:1510-30
47. Krings M. 2000. Remains of secretory cavities in pinnules of Stephanian pteridosperms from Blanzy-Montceau (Central France): A comparative study. Bot. J. Linn. Soc. 132:369-83
48. Krings M, Kellogg DW, KerpH,TaylorTN. 2003. Trichomes of the seed fern Blanzyopteris praedentata: implications for plant-insect interactions in the Late Carboniferous. Bot. J. Linn. Soc. 141:133-49
49. Krings M, Kerp H. 1998. Epidermal anatomy of Barthelopteris germarii from the Upper Carboniferous and Lower Permian of France and Germany. Am. J. Bot. 85:553-62
50. Krings M, Kerp H. 1999. Morphology, growth habit, and ecology of Blanzyopteris praedentata (Gothan) nov. comb., a climbing neuropteroid seed fern from the Stephanian of central France. Int. J. Plant Sci. 160:603-19
51. Krings M, Kerp H, Taylor TN, Taylor EN. 2003. How Paleozoic vines and lianas got off the ground: on scrambling and climbing Carboniferous-Early Permian pteridosperms. Bot. Rev. 69:204-24
52. Krings M, Taylor TN, Kellogg DW. 2002. Touch-sensitive glandular trichomes: A mode of defence against herbivorous arthropods in the Carboniferous. Evol. Ecol. Res. 4:779-86
53. Kroken SB, Graham LE, Cook ME. 1996. Occurrence and evolutionary significance of resistant cell walls in charophytes and bryophytes. Am. J. Bot. 83:1241-54
54. Labandeira CC, Tremblay SL, Bartowski KE, VanAller Hernick L. 2014. Middle Devonian liverwort herbivory and antiherbivore defence. New Phytol. 202:247-58
55. Lange BM, Ahkami A. 2013. Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes-current status and future opportunities. Plant Biotechnol. J. 11:169-96
56. Lange BM, Turner GW. 2013. Terpenoid biosynthesis in trichomes-current status and future opportunities. Plant Biotechnol. J. 11:2-22
57. Langenheim JH. 2003. Plant Resins: Chemistry, Evolution, Ecology, and Ethnobotany. Portland, OR:Timber
58. Lewinsohn E, Gijzen M, Savage TJ, Croteau R. 1991. Defense mechanisms of conifers: relationship of monoterpene cyclase activity to anatomical specialization and oleoresin monoterpene content. Plant Physiol. 96:38-43
59. Li G, Kollner TG, Yin Y, Jiang Y, Chen H, et al. 2012. Nonseed plant Selaginella moellendorffi has both seed plant and microbial types of terpene synthases. PNAS 109:14711-15
60. Li L, McCraig BC, Wingerd BA, Wang J, Whalon ME, et al. 2003. The tomato homolog of CORONATINE-INSENSITIVE 1 is required for the maternal control of seed maturation, jasmonatesignaled defense responses, and glandular trichome development. Plant Cell 16:126-43
61. LohrM, Schwender J, Polle JE. 2012. Isoprenoid biosynthesis in eukaryotic phototrophs: A spotlight on algae. Plant Sci. 185-86:9-22
62. Ma X, Gang DR. 2004. The Lycopodium alkaloids. Nat. Prod. Rep. 21:752-72
63. Mahlberg PG,FieldDW,Frye JS. 1984. Fossil laticifers from Eocene brown coal deposits of the Geiseltal. Am. J. Bot. 71:1192-200
64. Malcolm SB, Brower LP. 1989. Evolutionary and ecological implications of cardenolide sequestration in the monarch butterfly. Experientia 45:284-95
65. Martin D, Tholl D, Gershenzon J, Bohlmann J. 2002. Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol. 129:1003-18
66. Meslet-Cladière L, Delage L, Leroux CJ, Goulitquer S, Leblanc C, et al. 2013. Structure/function analysis of a type III polyketide synthase in the brown alga Ectocarpus siliculosus reveals a biochemical pathway in phlorotannin monomer biosynthesis. Plant Cell 25:3089-103
67. Miyazaki S, Katsumata T, Natsume M, Kawaide H. 2011. The CYP701B1 of Physcomitrella patens is an ent-kaurene oxidase that resists inhibition by uniconazole-P. FEBS Lett. 585:1879-83
68. Mizutani M, Ohta D. 2010. Diversification of P450 genes during land plant evolution. Annu. Rev. Plant Biol. 61:291-315
69. Napp-Zinn K. 1966. Anatomie des Blattes, Teil 1: Blattanatomie der Gymnospermen. Handb. Pflanzenanat. Vol. 8. Berlin: Gebr uder Borntraeger
70. Niklas KJ, Kutschera U. 2010. The evolution of the land plant life cycle. New Phytol. 185:27-41
71. Otto A, Wilde V. 2001. Sesqui-, di-, and triterpenoids as chemosystematic markers in extant conifers-a review. Bot. Rev. 67:141-238
72. Parsons HT, Christiansen K, Knierim B, Carroll A, Ito J, et al. 2012. Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol. 159:12-26
73. Patten AM, Vassão DG, Wolcott MP, Davin LB, Lewis NG. 2010. Trees: A remarkable biochemical bounty. In Comprehensive Natural Products II: Chemistry and Biology, Vol. 3: Development and Modification of Bioactivity, ed. L Mander, Liu HWB, pp. 1173-296. Oxford, UK: Elsevier
74. Petschenka G, Fandrich S, Sander N, Wagschal V, Boppr'e M, Dobler S. 2013. Stepwise evolution of resistance to toxic cardenolides via genetic substitutions in the Na+/K+-ATPase of milkweed butterflies (Lepidoptera: Danaini). Evolution 67:2753-61
75. PickardWF. 2008. Laticifers and secretory ducts: two other tube systems in plants. New Phytol. 177:877-88
76. Pollastri S, Tattini M. 2011. Flavonols: old compounds for old roles. Ann. Bot. 108:1225-33
77. Raffa KF. 2014. Terpenes tell different tales at different scales: glimpses into the chemical ecology of conifer-bark beetle-microbial interactions. J. Chem. Ecol. 40:1-20
78. Raffa KF, Hobson KR, LaFontaine S, Aukema BH. 2007. Can chemical communication be cryptic? Adaptations by herbivores to natural enemies exploiting prey semiochemistry. Oecologia 153:1009-19
79. Sabovljevi'c M, Vujici'c M, Sabovljevi'c A. 2014. Plant growth regulators in bryophytes. Bot. Serb. 38:99-107
80. Sallaud C, Rontein D, Onillon S, Jabès F, Duff'e P, et al. 2009. A novel pathway for sesquiterpene biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 21:301-17
81. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magall 'on S, Lupia R. 2004. Ferns diversified in the shadow of angiosperms. Nature 428:553-57
82. Smith EC, Griffiths H. 1996. A pyrenoid-based carbon-concentrating mechanism is present in terrestrial bryophytes of the class Anthocerotae. Planta 200:203-12
83. Sorensen I, Pettolino FA, Bacic A, Ralph J, Lu F, et al. 2011. The charophycean green algae provide insights into the early origins of plant cell walls. Plant J. 68:201-11
84. Stidd BM, Phillips TL. 1973. The vegetative anatomy of Schopfiastrum decussatum from the Middle Pennsylvanian of the Illinois Basin. Am. J. Bot. 60:463-74
85. Stirk WA, B'alint P, Tarkowsk'a D, Nov'ak O, Strnad M, et al. 2013. Hormone profiles in microalgae: gibberellins and brassinosteroids. Plant Physiol. Biochem. 70:348-53
86. SuireC,Bouvier F,Backhaus RA,B'eguD,BonneuM,CamaraB. 2000. Cellular localization of isoprenoid biosynthetic enzymes in Marchantia polymorpha. Uncovering a new role of oil bodies. Plant Physiol. 124:971-78
87. Thimmappa R, Geisler K, Louveau T, O'Maille P, Osbourn A. 2014. Triterpene biosynthesis in plants. Annu. Rev. Plant Biol. 65:225-57
88. Tissier A. 2012. Glandular trichomes:What comes after expressed sequence tags? Plant J. 70:51-68
89. Tittiger C. 2010. Pheromone production in bark beetles. Insect Biochem. Mol. Biol. 40:699-712
90. Van Schie CCN, Haring MA, Schuurink RC. 2007. Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol. Biol. 64:251-63
91. Vassão DG, Kim KH, Davin LB, Lewis NG. 2010. Lignans (neolignans) and allyl/propenyl phenols: biogenesis, structural biology, and biological/human health considerations. In Comprehensive Natural Products II: Chemistry and Biology, Vol. 1: Natural Products Structural Diversity-I: Secondary Metabolites: Organization and Biosynthesis, ed. L Mander, HWB Liu, pp. 815-928. Oxford, UK: Elsevier
92. Voo SS, Grimes HD, Lange BM. 2012. Assessing the biosynthetic capabilities of secretory glands in Citrus peel. Plant Physiol. 159:81-94
93. Walter MH, Strack D. 2011. Carotenoids and their cleavage products: biosynthesis and functions. Nat. Prod. Rep. 28:663-92
94. Warner KA,Rudall PJ, Fr ohlichMW.2009. Environmental control of sepalness and petalness in perianth organs of waterlillies: A new mosaic theory for the evolutionary origin of a differentiated perianth. J. Exp. Bot. 60:3559-74
95. Wasternack C, Hause B. 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111:1021-58
96. Wellman CH, Osterloff PL,Mohiuddin U. 2003. Fragments of the earliest land plants. Nature 425:282-85
97. Weng JK, Noel JP. 2013. Chemodiversity in Selaginella: A reference system for parallel and convergent metabolic evolution in terrestrial plants. Front. Plant Sci. 4:119
98. Wollenweber E, Schneider H. 2000. Lipophilic exudates of Pteridaceae-chemistry and chemotaxonomy. Biochem. Syst. Ecol. 28:751-77
99. Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP. 2010. Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr. Biol. 17:1225-30
100. Zulak KG, Bohlmann J. 2010. Terpenoid biosynthesis and specialized vascular cells of conifer defense. J. Integr. Plant Biol. 52:86-97