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The roles and hidden diversity o f e n d o p h y te f u n g i f r o m s p o tte d k n a p w e e d
Alexey Shipunov

P o s t- D o c to r a l R e s e a r c h S c ie n tis t D e p a r tm e n t o f F o r e s t R e s o u r c e s U n iv e r s ity o f I d a h o


Spotted knapweed

Spotted knapweed (Centaurea stoebe L., also known as C. maculosa, C. micrantha, C. biebersteinii) is a noxious, invasive plant which was introduced into North America from Eurasia. This plant is also a model in allelopathy research.


V o lg a r iv e r habitat

However, in native region (e.g., Russia and Ukraine), knapweed is not invasive.


Endophyte roles

Our goal is to explain knapweed invasiveness via plant-endophyte interactions


Hypotheses applicable to the k n a p w e e d i n v a s io n
· Enemy Release Hypothesis ­ enemies are left behind in the native range · Enhanced Mutualism Hypothesis ­ new symbionts obtained in the invaded range from native hosts ("host-jumping") and enhance abilities to compete natives, use resources etc. · Novel Weapons Hypothesis ­ many invasive North American plants have been reported to have antimicrobial, antiherbivore and allelopathic effects. These effects could be due to chemicals "unknown" for naОve native plants. Co-introduced symbionts may help to produce such an effect.


Catechin or not catechin

T h e m o s t a c c e p te d o p in io n ( C a lla w a y e t a l., 1999 and many others) is that cathechinc o n ta in e d k n a p w e e d r o o t e x u d a te s a r e c a p a b le to s u p p r e s s th e g r o w th o f n a tiv e g r a s s e s ( F e s t u c a, K o e l e r i a e t c . ) a n d o t h e r p l a n t s . H o w e v e r , r e c e n t e x p e r im e n ts ( B la ir e t a l., 2 0 0 5 , 2 0 0 6 ) s h o w th e a b s e n c e o f c a te c h in e ffe c t.


Negative interactions

Endophyte strain Fusarium 124 suppresses the flowering of knapweed


Some endophytes have almost pathogenic effect

T r a y s w ith in o c u la te d s e e d lin g s

T r a y s w ith c o n tr o l s e e d lin g s


Endophytes can suppress growth of Idaho fescue seedlings

The selective effect: terminate fescue much more than knapweed


Effects in seed assays
More than 2/3 endophyte strains have statistically significant termination effect on Festuca idahoensis seeds, some them have similar effect on knapweed seeds. Moreover, some endophytes can kill fescue seedlings.


Gas chromatogram: highest pike corresponds with sesquiterpene

Endophytes c a n p ro d u c e sesquiterpenes


Insecticide effect

In a choice experiment, biocontrol weevils Larinus minutus demonstrated strong preference to non-inoculated flowers


Attraction of aphids
Some endophytes can attract other knapweed-eaters: aphids

Green peach aphid Myzus persicae


Competition experiments
Differences in biomass are significant

E+ E­ knapweed knapweed and fescue and fescue

Fescue alone: control


Detailed competition experiment: fescue biomass

Novel weapons! Biomass of Festuca idahoensis decreased whereas biomass of F. ovina increased


K n a p w e e d b io m a s s
Some endophytes (Alternaria 73, Alternaria 432) definitely increase biomass whereas Epicoccum 66 decreases biomass along with plant height and number of flowers


Competitive advantage: the biomass difference

For nearly each pair of fescue species combined with particular endophyte, knapweed have competitive advantage over F. idahoensis much higher then over F. ovina


C o n c lu s io n : r o le s


Diversity: sampling

· · · · ·

61 knapweed populations sampled, plus 10 populations of native North American plants (Saussurea americana, Cirsium brevifolium, Festuca idahoensis etc.) 5 plants and 100 achenes per sample Endophytes isolated from achenes ­ 2291 isolates Isolates grouped in 288 morphological groups (strains) Each group has been sequenced (ITS and "Alt a 1"), 102 haplotypes obtained


Taxonomic and phylogenetic structure


BLAST identity and new species
Putative new species

# o f h a p lo ty p e s


Some endophytes may represent n o v e l l in e a g e s
Putative new species

Botrytis (anamorph of Botryitinia, Sclerotiniaceae)


The case of potential co-introduction: P h o m a t ra c h e ip h ila
The endophyte pho250 (South Germany) has 99% identity with GenBank sequences of Phoma tracheiphila, very dangerous pathogen of Citrus trees


Comparison of diversity between two ranges

Invaded range (N. America)

Native range (Europe)


Endemic and cosmopolitan haplotypes

Saussurea americana, American closest knapweed relative


Distribution of Botrytis 017/095 and C la d o s p o riu m 0 6 3


Ordination of communities
East U.S.

Cirsium brevifolium

Northern Idaho Principal coordinates analysis (PCO) based on Chao similarity indexes


Fungal haplotypes that characterize communities
Species are common for native range

Species are common for invaded range


Repeated sampling

Some of most widespread fungi are repeatedly isolated whereas some Alternaria species are not easy to re-isolate


Diversity and climate

We have higher isolation frequencies from sites where late summer and fall (August-November) precipitation is higher


Life cycle of knapweed endophytes (hypothesis)


Endophytes and invasion
Hypotheses of invasion Our research supports

E n e m y R e le a s e H y p o t h e s is E n h a n c e d M u t u a lis m H y p o t h e s is N ovel W eapons H y p o t h e s is

+ + +


Acknowledgements
·George Newcombe ·Anil Kumar Raghavendra ·Timothy Prather · Cort Anderson · Rebecca Ganley · Sanford Eigenbrode · Hongjian Ding · Maryse Crawford Web-site of the project: http://uidaho.edu/~shipunov