Constraints to the evolution of both insect and pathogen resistance in a wild

crucifer

Thure Hauser et al.University of Copenhagen

Barbarea vulgaris, flea beetles and white rust

Phyllotreta nemorumBarbarea vulgaris

Albugo candida

P

G

Insect resistance• Caused by specific tri-terpenoid saponin compounds

– Especially hederagenin cellobiocide

• Lethal to larvae– Rupture membrane of gut cells– Deterrent to adults if they taste it

• These saponins affect– Diamond Back Moth (Plutella xylostella)– Yellow-stiped flea beetle (Phyllotreta nemorum)– Some Pieris species and strains

– And probably other species as well

• The insect-susceptible plant type (P) produces other saponins with unknown function

OCH2OH

COOH

O

OH

HOO

HOH2C

O

OH

HOHO

HOH2C

White rust resistance • Resistance mechanism not known

– No correlation between Albugo and insect resistance in F3 hybrids

Frequency of plants with white rust symptoms

• Both the resistant and susceptible plant-types occur in Denmark– Why?

• If it is so great to be resistant, – why don’t we find only dually resistant

plants?

?

Historical constraints on evolution of dually resistant Barbarea plants?

• G and P type have different geographical distributions

Trait distributions

West East

Inse

ct re

sist

ance

Old historical divergence

• Thus, the different resistances of the G and P type are embedded in a larger divergence of the two types

• Diverged in different refugia during ice age?– Met later in Scandinavia and Finland

Reproductive barrier

G and P type is separated by a partial hybridisation barrier

Fully developed

Partially developed

Aborted

OCH2OH

COOH

O

OH

HOO

HOH2C

O

OH

HOHO

HOH2C

Proposed biosynthesis of saponins

oxidosqualene cyclases (OSC)

UDP-glycosyltransferases (UGT)

cytochrome P450 monooxygenases (P450)

O

HO HO

COOH

O

COOH

O

OH

HOHO

HOH2C

2,3-oxido-squalene

β-amyrinoleanolic

acid

hederagenin

hederageninmonoglucoside

oleanolic acidcellobioside

hederagenincellobioside

OSC

P450

UGT

oleanolic acidmonoglucoside

UGT

UGT

Common in all plants

O

COOH

O

OH

HOO

HOH2C

O

OH

HOHO

HOH2C

OCH2OH

COOH

O

OH

HOHO

HOH2C

P450 UGT

Recombining the insect and disease resistances into dually resistant plants is hindered by– Hybridisation barrier– Complex biosynthetic pathway that may be disrupted in hybrids

• A matter of time?

But is it really so great to be resistant?

!

?

Effect of resistances on F3 hybridsD

isease score in field

Bite

hol

esLe

af m

ines

Insect resistance

Pathogen resistance

Performance of F3 hybrids

• No fitness benefit of being insect resistant• Strong benefit of being disease resistant

Pathogen resistanceInsect resistance

Impact of flea beetles and white rustG-plants P-plants

New questions

• No obvious benefits of saponin-based insect resistance– Spectrum vs impact ?– Costs vs benefits?– Conditional on environment ?

• Why not only the pathogen-resistant P-type?– Disease incidence?– Time?

• Hybridisation barrier + trait associations– May have spread from the P-type to the G-type ?

– Genotype x environment interactions

?

Implications

• Present ecological interactions may be constrained by historical biogeography

• Defense traits and genes are not always beneficial for fitness– Use of resistances in biotech, breeding vs spraying ?

• Resistance-resources in wild crop-relatives

!

The Barbarea group

P-type

0

100

200

300

400

500

Contr Herb Path H&P

Sap

onin

3 (

peak

are

a)

.

0

20

40

60

80

Contr Herb Path H&P

G-type

0

50

100

150

200

250

300

Contr Herb Path H&P

Hederagenin cellobioside .

(peak area)

0

20

40

60

80

Contr Herb Path H&P

a

b

b

b

a a

c

b

Contr +Ins +Path +Both Contr +Ins +Path +Both

Induction of saponins (and glucosinolates)

• Saponins increase also in insect-resistant type• Combination of insect and pathogen gives highest induction

Oecologia, in press