How do plants deal with

biotic stress? Arthropods

HBC 206 Plant Biochemistry

Dr Fiona C Robertson
Department of Biochemistry
University of Zimbabwe
What are arthropods?
Horseshoe crabs
Arthropods are an
Arachnids (spiders and mites)
immense, diverse
Sea spiders group of
invertebrates
Centipedes and
millipedes
Some are terrestrial
Insects and others aquatic

Crustaceans Some mites and

insects are major
herbivores that can
cause extensive
damage to living
plants
 A long-term, complicated relationship
The basic conflict: Alliance #1:
plants are food for Most
herbivorous angiosperms rely Alliance #2:
arthropods upon arthropods Predatory or parasitic
for successful arthropods protect
reproduction plants from herbivore
damage

M. sexta eating N. attenuata

Nicotiana attenuata pollinated by
M. sexta after attack by predator
Manduca sexta moth

Photo credits: Danny Kessler; R.J. Reynolds Tobacco Company Slide Set, Bugwood.org; Wu, J., Hettenhausen, C., Meldau, S. and Baldwin, I.T. (2007). Herbivory
rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell. 19: 1096-1122.
 Plants and arthropods share 400
million years of evolution
Pollination

Simple Early leaf Leaf mining Nectar

piercing eating consuming

Plant diversity
Angiosperms

Gymnosperms,
cycads
Ferns

Million 400 300 200 100

years
ago
Image derived from : L. Shyamal based on work by Bruce Tiffney
 The ongoing conflict: Herbivory

Phloem-sucking Mesophyll-grazing Mesophyll- Root-vascular cylinder

aphids leaf miners sucking mites sucking nematodes

Leaf-chewing
larvae Plants produce
energy from
photosynthesis;
animals are
hungry and eat
plants
Photo credits: Sate Al Abbasi; David Cappaert, Michigan State University, Bugwood.org; University of Missouri. Published by MU Extension, all rights reserved. William Wergi; John R. Meyer, North Carolina State
University; Scott Bauer, USDA
Arthropods cause crop yield losses of
~10 - 30% every year

• How do arthropods damage

plants?

• How do plants defend

themselves from herbivores?

• How do herbivores cope with

plant defences?

Photo by Scott Bauer USDA

 Herbivory
Basic conflict – herbivory
Plant defence and herbivore counter-
measures
1. Constitutive defences
2. Induced defences
3. Secondary metabolites in defence
 1. Constitutive Defences

Physical Chemical Both

Chemical

Physical

Nicotine

Ranger, C.M., and Hower, A.A. (2001). Glandular morphology from a perennial alfalfa clone resistant to the potato leafhopper. Crop Sci. 41: 1427-1434.
 Physical defences against herbivory
Thorns
Trichomes (hairs)

Wax and wall Latex and resin

Waxy
cuticle

Cell
wall

Cardoso, M.Z. (2008). Herbivore handling of a Plant’s trichome: the case of Heliconius charithonia (L.) (Lepidoptera: Nymphalidae) and Passiflora lobata (Killip) Hutch. (Passifloraceae). Neotropical Entomology 37: 247-252.
From an arthropod’s perspective
trichomes can be lethal

Mentzelia pumila
trichomes and
trapped insects

Eisner, T., Eisner, M. and Hoebeke, E.R. (1998). When defense backfires: Detrimental effect of a plant’s protective trichomes on an insect beneficial to the
plant. Proc. Natl. Acad. Sci. USA 95: 4410-4414, copyright National Academy of Sciences, USA.
 Trichomes can release chemical
deterrents to arthropods
Tomato (Solanum Wild-potato
lycopersicum) (Solatium
berthaultii)
Pheromone-
or repellent-
releasing
trichome
Sticky-
releasing
Tomato trichomes trichome
produce chemicals
repellent to whiteflies

Wild-potato trichomes
Many trichomes produce aphid alarm
produce sticky pheromones
substances
Reprinted by permission from Macmillan Publishers Ltd. from Gibson, R.W., and Pickett, J.A. (1983).
Wild potato repels aphids by release of aphid alarm pheromone. Nature 302: 608-609.
 Latex can be avoided through vein
biting or trenching
Labidomera clivicollis cutting veins of Asdcepias syraca
prior to consuming distal tissues

Latex is sticky and often toxic. Herbivores

can cut the veins to drain out latex and
render the tissue edible

Dussourd, D., and Eisner, T. (1987). Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237: 898-901 reprinted with permission of AAAS.
2. Induced defences
Induced responses to herbivory

Plants resist herbivores through active

processes that include recognition of the
herbivore and defence responses to fight it

Perception Signal transduction Response

 Elicitors - Perception of herbivory
Biting and
wounding
damage

Piercing I-D-C-I
N Inceptin
and saliva G-V-C-V-D-A

Oral secretions Volicitin

and regurgitant

Egg laying
damage and
secretions
Phillip Roberts, USDA Forest Service University of Georgia, Bugwood.org; Mithöfer, A. and Boland, W. (2008). Recognition of herbivory-associated molecular patterns. Plant Physiology. 146: 825-831; .
Volicitin and inceptin are herbivory-
specific compounds
Volicitin is produced from
the conjugation of a plant-
derived fatty acid
conjugated to glutamine in
the herbivore midgut, then
regurgitated onto plant
tissues
I-D-C-I
N Inceptin
G-V-C-V-D-A
Inceptin is a peptide derived
from proteolytic cleavage by the
insect of a chloroplastic ATP
synthase from the plant
 Elicitors

Protein kinases

Perception of the herbivore

leads to a signal transduction
cascade that induce plant
defences
Herbivore signals induce expression of
secondary metabolite biosynthetic
genes and other defence & repair
genes

Wu, J., Hettenhausen, C., Schuman, M.C. and Baldwin, I.T. (2008). A comparison of two Nicotiana attenuata accessions reveals large differences in signaling induced by oral secretions of the specialist herbivore
Manduca sexta. Plant Physiology. 146: 927-939.
Many induced defence responses are
mediated by hormones
Hormone dependent Ethylene
signalling (ET)

Jasmonate
(JA) Salicylic acid
(SA)

• Direct responses (e.g. toxins)

• Indirect responses (e.g.
predator attraction)
Hormone-independent
signalling
Phillip Roberts, USDA Forest Service University of Georgia, Bugwood.org
 Herbivory induces direct and indirect
defences
Local signals Induction of direct defences
and hormone (e.g. alkaloids and other toxins,
proteinase inhibitors)
accumulation

Induction of volatiles
that attract natural
enemies of herbivores
(indirect defences)
 Herbivory induces defences locally and
systemically
Local signals Induction of
volatiles that
and hormone
attract natural
accumulation enemies of
herbivores
(indirect defences)

Long distance Induction of direct

signals and defences but a bit later
systemic responses and not as strong
 Some herbivores can suppress induced
plant defence responses

Tetranychus urticae Tetranychus evansi T. urticae and T. evansi together

T. urticae induces T. evansi suppresses The fitness of T. urticae increases in

tomato defences and induced defences in the presence of T. evansi
its fitness on tomato is tomato and is a
moderate serious pest on it

Some, but not all, spider mite species suppress or delay plant defences

Photo: Jan van Arkel (IBED; University of Amsterdam)

3. Secondary metabolites in defence
• Plants produce >100 000 compounds
• 80% of the known natural compounds have a
botanical origin Coumarins
• Many of these
Carbohydrate
chemicals function metabolism
in defence
• Many defence Photo-
synthesis
compounds are
secondary
metabolites
Alkaloids
Some secondary compounds attract
pollinators, predators or parasitoids

Aroma
pollinator

Odor

parasitoid

Color
predator

herbivore

Nectar
Photo source: Klaus Bolte, Natural Resources Canada Ottawa, Ontario, Canada
 Other compounds are toxic, or can be
converted to toxins, or are anti-nutritive
A cyanogenic glycoside
that releases toxic HC N
cyanide
Cyanide

Nicotine, a toxin Anti-nutritives interfere

found in tobacco and with herbivores’ digestion
its relatives or assimilation of
nutrients, impairing their
growth, development and
reproduction
 Some herbivores have evolved
tolerance to plant toxins
Herbivores can tolerate plant toxins
Sequestration through degradation, excretion and
toxin sequestration (through chemical
modification and storage in
Rapid specialized glands).
degradation Rapid
excretion In some cases the target enzyme has been
modified to now be unaffected by the toxin
Target Modified
(e.g. enzyme) target

toxin

toxin
 Defensive secondary metabolites can be
divided in three groups
Phenolics: e.g. Flavonoids, Salicylic acid, Lignins

Coumarins

Carbohydrate
metabolism

Photo-
synthesis

Nitrogen containing: Terpenoids:

e.g. Alkaloids and e.g. Limonoids
Alkaloids Saponins
Glucosinolates
Pinene
Phenolics and terpenes include medicines,
insecticides and irritants
Taxol is an anti-cancer
Pyrethrin is an Urushiol is an
drug from the Pacific
insecticide from allergen from
yew tree
Chrysanthemum poison ivy

Photo credit: Dave Powell, USDA Forest Service, Bugwood.org

And at least 10,000 more, many uncharacterized
 Some terpenoids, when induced can
attract predatory arthropods
CH3

H3 C CH2
limonene

CH3

OH
CH3
H3 C
menthol
Herbivore induced terpenes
Constitutive terpenes
Photo credit: Ted Turlings
 Alkaloids contain nitrogen and
include stimulants and narcotics
Theobromine Coffee
Coca
caffeine

Cocaine

Cacao

Nicotine Morphine
Tobacco Opium Poppy
Glucosinolates are typical for the
Cabbage (Brassicaceae) Family
 Myrosinases and glucosinolates are
stored in separate plant cells
Glucosinolates

Myrosinases
When the cells are
broken the two are
mixed, for example by
herbivore damage
Various toxic and
distasteful breakdown
products are produced
that deter most
herbivores
BUT Herbivores are constantly adapting to
plant defences

The diamondback moth

sulfatase enzyme removes
The Cabbage white the glucosinolate’s sulfate
butterfly larvae group such that myrosinase
sequester the does not recognize the
glucosinolates as glucosinolate
protection against anymore
predators
 Heliconian butterflies and passion
flowers
The larvae of more than 60 Passionflower
species of Heliconius plants make
butterflies are specialized structures
feeders of Passiflora and are that resemble
tolerant of their various butterfly eggs
secondary metabolites

Female butterflies prefer to lay

their eggs on an unoccupied
leaf to protect their young
from cannibals and avoid
leaves with ‘fake’ eggs
Ingested secondary defence compounds
can be toxic but sometimes herbivores
have adapted

Health
problems Sequestration
toxin

Rapid degradation Rapid

or conversion excretion
 Herbivores and crops
• Defence compounds are often toxic to humans
too eg cyanide in Cassava, glycoalkaloids in wild
potatoes

• They cost the plant a lot of energy to produce

• Many defences were lost, deliberately or not,

during breeding, making crops vulnerable to
pests
 Herbivore-resistant crops
• Maize, cotton, poplar, potato, rice, soybean and
tomato have been transformed to express the ‘Bt
gene’

• The ‘Bt gene’ is a gene from the bacterium Bacillus

thuringiensis

• The Bt protein is toxic to some types of insect

• Bt crops are now grown all over the word

 Alliance #1 – Plants and Carnivores or
Parasitoids
Hyposoter ebeninus attacking a
Lady beetle Assassin bug
Pieris rapae larva
devours a
pea aphid

Spider Parasitoid larvae Pirate bug eating aphid

mite and
predatory
mite (and
their eggs)

Parasitized caterpillar
Photo: T. Bukovinszky / www.bugsinthepicture.com; Thailand IPM; R.J. Reynolds Tobacco Company Slide Set , Bradley Higbee, Paramount Farming; Bugworld.org; Scott Bauer, USDA
Alliance #2 – Plants and Pollinators

Christian Konrad Sprengel (1793) “Das entdeckte Geheimnis der Natur im Bau und in der Befruchtung der Blumen”
Which floral cues are most important?

Petunia axillaris Petunia integrifolia Petunia exserta

Three closely related petunias are pollinated by moths,

bees and hummingbirds

Hoballah, M.E., Gübitz, T., Stuurman, J., Broger, L., Barone, M., Mandel, T., Dell'Olivo, A., Arnold, M., and Kuhlemeier, C. (2007). Single gene-mediated shift in
pollinator attraction in petunia. Plant Cell 19: 779-790; Reprinted from Klahre et al., (2011) Pollinator choice in petunia depends on two major genetic loci for floral
scent production, Curr. Biol. 21: 730-739 with permission from Elsevier.
 Which cues are most important?

Petunia axillaris Petunia integrifolia Petunia exserta

Moth Bee Hummingbird
White petals Violet petals Red petals
Strong fragrance Little fragrance Little fragrance
Abundant nectar Little nectar Abundant nectar
Long tube Short tube Exserted sexual organs

Hoballah, M.E., Gübitz, T., Stuurman, J., Broger, L., Barone, M., Mandel, T., Dell'Olivo, A., Arnold, M., and Kuhlemeier, C. (2007). Single gene-mediated shift in
pollinator attraction in petunia. Plant Cell 19: 779-790; Reprinted from Klahre et al., (2011) Pollinator choice in petunia depends on two major genetic loci for floral
scent production, Curr. Biol. 21: 730-739 with permission from Elsevier.
 Summary

Many of the
compounds that
contribute to plant
direct and indirect
defences have been
identified, opening up
the possibility to
engineer plants with
enhanced defences

Reprinted from Dicke, M., and Baldwin, I.T. (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci. 15: 167-175, with permission from Elsevier.