The biology of Melampsora larici-

populina

Pascal FreyINRA NancyJoint Research Unit « Tree – Microbe Interactions »Champenoux, France

Melampsora Genome Consortium - 2008 Summer Workshop

Poplar rust is caused by several Melampsora spp.

Main disease in commercial poplar cultivation worldwide

Symptoms :

• perturbation of photosynthesis

• early defoliation

• reduction of biomass

High yield losses

• perturbation of automnal translocation

• susceptibility to secondary parasites

Death of young trees

Why sequencing poplar rust ?

© Jean Pinon, INRA Nancy

• low number of cultivars planted (less than 5 per region)

• monoclonal and even-aged plantations

• large spacing plantations: peeling (veneer, packaging), sawing, particle boards

• Short Rotation Coppice (SRC): biomass and bioenergy

• France is the first poplar wood producer in the EU (ca. 2.5 millions m3/yr)

P. nigra P. trichocarpaP. deltoides

euramerican hybrids

interamerican hybrids

Poplar cultivation in Europe

A few botanical facts about the genus Populus

Genus Populus :Class : EudicotylédonesClade : Eurosidae IOrder : MalpighialesFamily : Salicaceae (genus Salix and Populus)

Between 29 and >100 species according to different authors.

Eckenwalder’s (1996) classification is widely accepted.Eckenwalder JE (1996) Systematics and evolution of Populus. In Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (Eds), Biology of Populus and its implications for management and conservation, Chap. 1. pp. 7-32. NRC Research Press, Ottawa, Canada.

The genus Populus comprises 6 sections, clustering intercrossing species (also a few cases of inter-sectionnal intercrosses)

The 6 sections among the genus Populus according to Eckenwalder (1996)

NB: P. maximowiczii = P. suaveolens s.l.

Section Espèce Origine Section Espèce Origine

Aigeiros P. nigra Eurasie P. alba Eurasie

(noirs) P. deltoides Amérique Nord P. tremula Eurasie

P. fremontii Amérique Nord P. tremuloides Amérique Nord

P. trichocarpa Amérique Nord Populus P. grandidentata Amérique Nord

P. balsamifera Amérique Nord (ex-Leuce ) P. guzmanantlensis Mexique

P. angustifolia Amérique Nord P. monticola Mexique

Tacamahaca P. ciliata Himalaya P. sieboldii Asie

(baumiers) P. laurifolia Eurasie P. simaroa Mexique

P. simonii Chine P. gamblei Himalaya

P. suaveolens Asie P. adenopoda Chine

P. szechuanica Chine P. euphratica Eurasie, Afrique

P. yunnanensis Chine Turanga P. ilicifolia Afrique

P. lasiocarpa Chine P. pruinosa Asie

Leucoides P. glauca Asie Abaso P. mexicana Mexique

P. heterophylla Amérique Nord

P. nigra (N) P. trichocarpa (T)P. deltoides (D)

P. x euramericana (syn. P. x canadensis)

(DxN)e.g. 'Robusta', 'I214'

P. x interamericana (syn. P. x generosa)

(DxT or TxD)e.g. 'Beaupré'

The euramerican and interamerican hybrids

Rust fungi are excellent botanists !

  

  Aigeiros Tacamahaca Populus

Melampsora spp.P.

nigraP.

deltoidesP.

trichocarpaP.

albaP.

tremulaP.

tremuloides

  M. larici-populina + + + - - -

  M. allii-populina + + + - - -

  

M. medusae f. sp. deltoidae + + - - - -

M. occidentalis ? - + - - -

  M. pinitorqua - - - + + ?

  M. rostrupii - - - + + ?

  M. larici-tremulae - - - + + ?

  M. magnusiana - - - + + ?

  M. pulcherrima - - - + ? ?

 M. medusae f. sp. tremuloidae

- - - ? ? +

The taxonomic position of Melampsora larici-populina

Wingfield et al 2004 Austral. Plant Pathol.

Basidiomycota

Pucciniomycotina

Pucciniomycetes

Pucciniales (= Uredinales)

Melampsoraceae

Melampsora

larch

poplar

telia andteliospores (n+n)

aecidia (n+n)

plasmogamy

aecidiospores (n+n)

basidiospores (n)

spermogoniaand spermatia (n)

uredinia andurediniospores (n+n)

The life cycle of Melampsora larici-populina: a heteroecious macrocyclic rust

meiosiscaryogamy

basidia (2n)

++

--

X

++

--

X

sexual reproductionpoplar-larch sympatrymonocyclic3 weeks

asexual reproductionepidemic phase polycyclic5 months

The life cycle of Melampsora larici-populina: a heteroecious macrocyclic rust

teliaspermogonia

aecia uredinia

basidia

PoplarLarch

© P. Frey, INRA

© P. Frey, INRA

© P. Frey, INRA

© P. Frey, INRA

© P. Frey, INRA

The life cycle of Melampsora larici-populina:

The life style of Melampsora larici-populina: a strict biotrophic fungus

• M. larici-populina needs fresh plant tissue (poplar leaves) to grow on • Numerous attempts to find artificial culture media for rust fungi, but with limited success (limited mycelial growth, but no infectious spores produced)

• likely due to a very specific interface between the pathogen and the host tissues: the haustorium

© Stéphane Hacquard, INRA

Matthias Hahn, 2000

The infection process of Mlp: a « lazy » fungus

The infection process of Mlp: a « lazy » fungus

Laurans & Pilate, 1999, Phytopathology 89: 233-238

2 hrs post inoculation

Rinaldi et al., 2007 Plant Physiol. 144: 347-366

7 days post inoculation

The Populus-Mlp interaction: a gene-for-gene model

• H.H. Flor 1942: « Each dominant resistance gene in the host plant matches a dominant avirulence gene in the pathogen »

• GFG relationship is very likely in the Populus-Mlp interaction, but not demonstrated yet

• At least 8 qualitative (major) rust resistance genes described in poplar, and 8 avirulence loci in Mlp:

8 virulence loci 28 = 256 possibles pathotypes

Strain 98AG31: Vir3-Vir4-Vir7(Avr1, Avr2, Avr5, Avr6, Avr8)

Mlp has overcome almost all the R genes released

• Examples:1986: breakdown of R3 ('Luisa-Avanzo')1994: breakdown of R7 ('Beaupré')1997: breakdown of R8 ('Hoogvorst')

• In 2008, of the 130 cultivars available in the UE, only one recently released cv. is completely resistant to Mlp

• Dispersal of Vir7 after the breakdown of R7

1994 1995 1996 1997 1998 1999

(Pinon et al. 1998)

Mlp has great dispersal capacities

• regional scale: the Durance River valley

• national scale:dispersal of Vir7 in France

• intercontinental scale:Iceland 1999Canada 2002

Wild poplar riparian stands

Poplar-larch sympatry area

annual epidemic annual epidemic

Prelles

St Clément

Rochebrune

Monêtier

Valernes

Les Mées

La Brillanne

Mirabeau

Châteauroux

Embrun

BPR Pont du Fossé

BPR Manse

BPR Manosque

BPR Valernes

BPR Mirabeau

Cultivated poplar stands (R7)

Durance

15 km

Mlp is among pathogens with highest evolutionnary risk

Linde & McDonald, 2002, Annu. Rev. Phytopathol.

A nomenclatural issue about Mlp:

Klebahn, 1902. Kulturversuche mit Rostpilzen Z. PflKrankh. PflPath. PflSchutz 12: 43First description of the heteroecious rust fungus M. larici-populina (M. populina = Caeoma laricis)

Saccardo P.A. (1905) Sylloge Fungorum 17: 463 M. laricis-populina

A nomenclatural issue about Mlp:

• All the literature of the 20th century concerning Mlp used the spelling M. larici-populina

• In 1997, first ITS sequences deposited in GenBank: they use the spelling M. laricis-populina, according to the Index Fungorum

•Taxonomy browser of GenBank :•M. larici-populina : MycoBank (www.mycobank.org)•M. laricis-populina : Index Fungorum (www.indexfungorum.org) and USDA-ARS Systematic Mycology and Microbiology Laboratory, Fungal Databases (http://nt.ars-grin.gov/fungaldatabases)

• DoE JGI portal for Mlp : M. laricis-populina !

• according to some latinists, both can be correct, depending if one considers that larici is an hyphenation of laricis, or that the genetive laricis should apply