Genetic diversity, host relationships, and bioclimatic modeling to predict potential global distribution of the myrtle rust pathogen

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1 Genetic diversity, host relationships, and bioclimatic modeling to predict potential global distribution of the myrtle rust pathogen Ned B. Klopfenstein USDA Forest Service, Rocky Mountain Research Station, Moscow, Idaho U.S.A J.E. Stewart, M.-S. Kim, P.G. Cannon, A.L. Ross-Davis, J.W. Hanna, E.W.I. Pitman, R.N. Graҫa, A.C. Alfenas, T.L. Peever, J.Y. Uchida, R.D. Hauff, C.Y. Kadooka, S. Namba, S. Simeto, C.A. Pérez, M.B. Rayamajhi, D.J. Lodge, M. Arguedas, R. Medel-Ortiz, M.A. López-Ramirez, P. Tennant, M. Glen, P. da S. Machado, A.R. McTaggart, and A.J. Carnegie Myrtle Rust Symposium, New Zealand Invasive Species Working Group, Better Border Biosecurity (B3), New Zealand Institute for Plant and Food Research Ltd., 28 August 2017, Auckland, New Zealand

Austropuccina psidii Primary example of an emerging forest disease caused by rust pathogen Biotrophic rust fungus Infects young, actively growing foliage, floral buds, and young fruits of host

2 Austropuccina psidii Primary example of an emerging forest disease caused by rust pathogen Biotrophic rust fungus Infects young, actively growing foliage, floral buds, and young fruits of host species in the Myrtaceae Unusually wide host range (450+ species; 33+ genera) Brown lesions with masses of yellow or orange urediniospores; dark brown teliospores; purpling with age Decreased growth; loss of apical dominance Native to South and Central America? Several races or biotypes

3 Life Cycle Glen et al., 2007

4 Austropuccinia psidii - Host range examples Angophora Callistemon Corymbia Eucalyptus Eugenia Heteropixis Marlierea Melaleuca Metrosideros Myrcia Myrciaria Pimenta Psidium Syzigium From: A.C. Alfenas

composition, and function of forests http://www.hear.

5 Threats of myrtle rust Susceptible species are often dominant components of flora in Oceania, Southeast Asia, South and Central America, and southern Africa outbreaks change structure, composition, and function of forests >700 species of Eucalyptus, mostly native to Australia most widely planted genus

6 Reports of Austropuccinia psidii occurrence Brazil 1884: guava First report

7 Reports of Austropuccinia psidii occurrence Jamaica 1934: allspice, rose apple, (did not infect guava) Colombia 1926: rose apple Puerto Rico 1912: rose apple Brazil 1884: guava 1902: rose apple 1912: eucalypt

8 Reports of Austropuccinia psidii occurrence Hawaii, USA 2005: Ohi a Jamaica 1934: Rose apple, Allspice Colombia 1926: rose apple Florida, USA 1977: Allspice Puerto Rico 1912: Rose apple Brazil 1884: Guava 1912: Eucalypt : Rose apple, 1973: Serious outbreak in eucalypt plantations Hainan, China 2009: Rose apple Indonesia 2015: Eucalypt, Melaleuca South Africa 2013: Myrtus communis Australia 2010: diverse Myrtaceae Japan 2007: Ohi a (nursery) Taiwan 1992: eucalypt (not established) New Caledonia 2013: Rose apple New Zealand 2017: Metrosideros

9 Several examples of new reports of myrtle rust around the world

10 What are the genetic similarities and differences among Austropuccinia psidii genotypes that infect diverse hosts in widely ranging global areas? = Austropuccinia psidii occurrence From: A.C. Alfenas

11 Characterization of Austropuccina psidii populations in Brazil HYPOTHESIS: A. psidii jumped from guava to eucalypts shortly after their introduction to Brazil Guava (Psidium guajava) Eucalypt (Eucalyptus spp.) Graça et al Mol Ecol 22:

(Allele 1)---CACACACACACACACACA--- = (CA)9

12 Population genetics approaches to understand Austropuccinia psidii ecology and improve threat assessments. (Allele 2)---CACACACACACACACA---- = (CA)8 (Allele 1)---CACACACACACACACACA--- = (CA)9 Precise collection information (e.g., host, GPS coordinates, date, etc.) Host range tests DNA extraction and PCR Microsatellite (SSR) sequencing and analyses

13 Austropuccinia psidii collections in Brazil Brazil # samples Host 70 Eucalypt 63 Guava (Psidium guajava) 4 Rose apple (Syzygium jambos) 2 Brazilian guava (P. guineense) 4 Java plum (S. cumini) 3 Jabuticaba (Myrciaria cauliflora) 2 Pitanga (Eugenia uniflora) Single pustule isolation Graça et al Mol Ecol 22:

14 Microsatellite genotyping of Austropuccinia psidi isolates (Allele 2)---CACACACACACACACA---- = (CA)8 (Allele 1)---CACACACACACACACACA--- = (CA)9 DNA extraction and PCR 10 microsatellite loci were scored for 148 A. psidii isolates, which revealed 25 unique multilocus genotypes

15 Principal coordinates analysis 25 unique Austropuccinia psidii genotypes Guava and Brazilian guava Eucalypt and rose apple Graça et al Mol Ecol 22:

16 Population structure of 148 Austropuccinia psidi isolates from seven myrtaceous hosts in Brazil STRUCTURE v2.3.4 Graça et al Mol Ecol 22:

Six evolutionary scenarios modeled in DIYABC 1-100,000 years 1-1000 years 1-100,000 years 1-1000 years Assuming two populations, an older divergence event between guava- and eucalyptassociated

17 Six evolutionary scenarios modeled in DIYABC 1-100,000 years years 1-100,000 years years Assuming two populations, an older divergence event between guava- and eucalyptassociated populations (Scenario 2) had a significantly higher posterior probability (0.9932) than divergence between guava- and eucalypt-associated populations within the last 1000 years (Scenario 1; ) Assuming three populations, a more recent divergence of eucalypt-associated population from the other population (Scenario 4) had significantly higher posterior probability (0.9836) than a more recent divergence event between guava- and eucalypt-associated populations (Scenario 3; )

18 Conclusions - Brazil study Austropuccinia psidii infections of eucalypt in Brazil did not originate via a host shift from guava; A. psidii is differentiated by host in Brazil, with at least two genotypically distinct biotypes; and Divergence between the two biotypes within the past 1000 years is highly unlikely

19 How does genetic diversity of Austropuccinia psidi in Central/North America and Hawaii compare with that found in Brazil and Uruguay?

20 Geographic origin, host, and genetic cluster of Austropuccinia psidii samples. 1 Bayesian analysis of population structure (BAPS) identified nine genetic clusters (C1 C9) among 226 Austropuccinia psidii isolates. Origin Host N BAPS cluster 1 Brazil Eucalyptus spp. 70 C2 and C3 Eugenia uniflora 2 C7 Myrciaria cauliflora 3 C9 Psidium guajava 63 C6 Psidium guineenese 2 C6 Syzygium cumini 4 C5 Syzygium jambos 3 C2 Costa Rica Callistemon lanceolatus 2 C1 Jamaica Pimenta dioica 6 C8 Syzygium jambos 4 C1 Mexico Syzygium jambos 1 C1 Puerto Rico Syzygium jambos 1 C1 Uruguay Eucalyptus grandis 1 C2 Eucalyptus globulus 3 C2 Myrrhinium atropurpurea 1 C8 USA - Florida Melaleuca quinquenervia 5 C4 Myrcianthes fragrans 1 C4 Rhodomyrtus tomentosa 2 C4 Syzygium jambos 2 C4 USA - Hawaii Eugenia koolauensis 3 C1 Melaleuca quinquenervia 4 C1 Metrosideros excelsa 1 C1 Metrosideros polymorpha 9 C1 Myrtus communis 1 C1 Rhodomyrtus tomentosa 2 C1 Syzygium cumini 1 C1 Syzygium jambos 28 C1 Syzygium malaccense 1 C1 226

Population structure of 226 Austropuccinia psidii samples Population structure of 226 Austropuccinia psidii samples inferred using a Bayesian clustering algorithm implemented in BAPS with each

21 Population structure of 226 Austropuccinia psidii samples Population structure of 226 Austropuccinia psidii samples inferred using a Bayesian clustering algorithm implemented in BAPS with each individual represented by a vertical line partitioned into shaded segments corresponding to the isolate s estimated mean membership coefficient for K = 9 genetic clusters; mean LnP(K) =

22 Principal coordinates analysis of 226 Austropuccinia psidii samples Principal coordinates analysis of the 23 mutlilocus genotypes of 226 Austropuccinia psidii isolates among nine clusters (C1 C9) as identified by BAPS based on a covariance matrix with data standardization. The first two axes explain 79% of the observed variation.

23 Minimum-spanning network of Austropuccinia psidii microsatellite multilocus genotypes (MLGs) samples from Brazil (BR) Costa Rica (CR) Jamaica (JM) Mexico (MX) Puerto Rico (PR) Uruguay (UR) Florida (FL) USA Hawaii (HI) USA on 18 hosts. MLGs are represented by BAPS genetic clusters: C1 represents MLGs from Costa Rica on crimson bottlebrush (Callistemon lanceolatus), Jamaica, Mexico, Puerto Rico on rose apple (Syzygium jambos) and Hawaii, USA on koʻolau eugenia (Eugenia koolauensis), broad-leaved paperbark (Melaleuca quinquenervia), pōhutukawa (Metrosideros excelsa), ʻōhiʻa lehua (M. polymorpha), common myrtle (Myrtus communis), rose myrtle (Rhodomyrtus tomentosa), Java plum (S. cumini), rose apple and Malay rose apple (S. malaccense); C2 represents MLGs collected from Brazil on eucalypts (Eucalyptus spp.) and rose apple and from Uruguay on eucalypts (Eucalyptus grandis and E. globulus); C3 represents one MLG collected from Brazil on eucalypts; C4 represents MLGs collected from Florida, USA on broad-leaved paperbark, twin berry (Myrcianthes fragrans), rose myrtle and rose apple); C5 represents one MLG collected in Brazil on Java plum; C6 represents one MLG collected in Brazil on guava (Psidium guajava)and Brazilian guava (P. guineense); C7 represents one MLG collected in Brazil on pitanga (Eugenia uniflora); C8 represents MLGs collected from Jamaica on allspice (Pimenta dioica) and Uruguay on sweet flower (Myrrhinium atropurpureum); C9 represents one MLG collected from Brazil on jabuticaba (Myrciaria cauliflora). Sizes of circles are proportional to MLG frequency. Connections are labelled with Bruvo genetic distances if different from 0.04, which corresponds to 1 mutational step at one locus. Broken lines connect MLGs that are separated by distances >0.20. Loops with dotted lines in the network (i.e., with C1-, C5-and C8-associated MLGs) indicate multiple, tied minimum-spanning trees

24 At least three biotypes are represented within the minimum-spanning network C1 and C4: Pandemic diverse hosts in diverse regions C6: Guava/Brazilian Guava - Brazil Allspice Jamaica Biotype?? C2 and C3: eucalypt/rose apple Brazil/Uruguay

25 Others have confirmed that the Pandemic biotype of Austropuccina psidii occurs in Australia, China (Hainan), New Caledonia, Indonesia, and Colombia Machado et al Austalasian Pl. Pathol. 44: McTaggart et al Austalasian Pl. Pathol. 45: Granados et al Austalasian Pl. Pathol. 46:

Bioclimatic modeling of Austropuccinia psidii MaxEnt models of suitable climate space (potential distribution) for Austropuccinia psidii based on 19 global bioclimatic variables derived from the

26 Bioclimatic modeling of Austropuccinia psidii MaxEnt models of suitable climate space (potential distribution) for Austropuccinia psidii based on 19 global bioclimatic variables derived from the WorldClim (worldclim.org) database (A) All genotypes (N = 403) (B) C1/C4 biotype (Pandemic: occurrence points from diverse hosts in Costa Rica, Jamaica, Mexico, Puerto Rico, USA- Hawaii/Florida and Australia; N = 137) (C) C2/C3 biotype (eucalypt/rose apple Brazil/Uruguay; N = 80) (D) C6 biotype (guava/brazilian guava Brazil; N = 60)

C1/C4 biotype (Pandemic: occurrence points from diverse hosts in Costa Rica, Jamaica, Mexico, Puerto

27 MaxEnt models of suitable climate space (potential distribution) for Austropuccinia psidi in Hawaii, USA (A) All genotypes (N = 403) (C) C2/C3 biotype (eucalypt/rose apple Brazil/Uruguay; N = 80) (B) C1/C4 biotype (Pandemic: occurrence points from diverse hosts in Costa Rica, Jamaica, Mexico, Puerto Rico, USA-Hawaii/Florida and Australia; N = 137) (D) C6 biotype (guava/brazilian guava Brazil; N = 60)

guajava P. araca UFV2 Euba1 M. caulif. P. guajava P. araca Brazilian A. psidii strains The Brazilian A.

28 Assessment of Brazilian Austropuccinia psidii biotype virulence to Hawaiian ohi a (Metrosideros polymorpha) Mean severity of ohi a leaf damage 20 Control vs inoculated Severity % UFV2 Euba1 M. caulif. P. guajava P. araca UFV2 Euba1 M. caulif. P. guajava P. araca Brazilian A. psidii strains The Brazilian A. psidii eucalypt/rose apple biotype was highly virulent on Hawaiian ohi a plants Silva et al Pacific Science 68: 47-56

2014) Hawaii possesses suitable climate space for the A. psidii eucalypt/rose apple biotype from Brazil The A.

29 Threat assessment of Austropuccinia psidii eucalypt/rose apple biotype to native ohi a in Hawaii Hawaiian ohi a plants are very susceptible to A. psidii eucalypt/rose apple biotype from Brazil (Silva et al. 2014) Hawaii possesses suitable climate space for the A. psidii eucalypt/rose apple biotype from Brazil The A. psidii eucalypt/rose apple biotype from Brazil likely poses a major threat to native ohi a in Hawaii, should this biotype ever be introduced.

MaxEnt models of suitable climate space (potential distribution) for Austropuccinia psidi in Australia, New Zealand, and adjacent regions (A) All genotypes (N = 403) (C) C2/C3 biotype (eucalypt/rose

30 MaxEnt models of suitable climate space (potential distribution) for Austropuccinia psidi in Australia, New Zealand, and adjacent regions (A) All genotypes (N = 403) (C) C2/C3 biotype (eucalypt/rose apple Brazil/Uruguay; N = 80) (B) C1/C4 biotype (Pandemic: occurrence points from diverse hosts in Costa Rica, Jamaica, Mexico, Puerto Rico, USA-Hawaii/Florida and Australia; N = 137) (D) C6 biotype (guava/brazilian guava Brazil; N = 60)

Example assessment of potential threats posed by eucalypt/rose apple (Brazil/Uruguay) biotype of

(2010) showed that several myrtaceous species from Australia were susceptible to A.

and part of New Zealand have suitable climate space for A.

31 Example assessment of potential threats posed by eucalypt/rose apple (Brazil/Uruguay) biotype of Austropuccinia psidi if introduced to Oceania A previous study by Zauza et al. (2010) showed that several myrtaceous species from Australia were susceptible to A. psidii eucalypt/rose apple biotype from Brazil Bioclimatic modelling indicates that eastern Australia and part of New Zealand have suitable climate space for A. psidii eucalypt biotype Australia The eucalypt/rose apple biotype of A. psidii from Brazil/Uruguay likely represents a threat to several myrtaceous species in regions of Oceania, including New Zealand

Climate change will influence the distribution of Austropuccinia psidii An example of climate-change predictions for South America Current 2050 Predicted current (based on years

psidii in South America for the 2050s (years 2040-2069) using CCCMA-CGCM global circulation model and A1B SRES emissions scenario.

32 Climate change will influence the distribution of Austropuccinia psidii An example of climate-change predictions for South America Current 2050 Predicted current (based on years ) suitable climate space for A. psidii in South America based on 169 occurrences. Model projection of suitable climate space for A. psidii in South America for the 2050s (years ) using CCCMA-CGCM global circulation model and A1B SRES emissions scenario. These predictions used MaxEnt and 19 bioclimatic surfaces from WorldClim. The dark green represents areas with suitable climate for A. psidii, with light green, yellow, orange, and red indicating increased suitability, respectively (From Klopfenstein et al. 2011)

33 Summary Austropuccinia psidii is an invasive rust pathogen that appears to comprise at least 9 genetic clusters (C1-C9). The C1/C4 clusters ( Pandemic biotype ) associated with diverse hosts in many geographic regions. Each A. psidii biotype (e.g., C1/C4, C2/C3, and C6) has different ecological behavior, in terms of associated hosts and suitable climate space (potential distribution). An understanding of A. psidii biotypes/genotypes is essential for tracking pathogen spread, conducting threat assessments developing regulatory measures, and implementing management strategies for this invasive pathogen.

34 Many questions remain What is the role of climate change in the emergence of myrtle rust? What is the role of sexual reproduction in the adaptation of A. psidii? What is the adaptive capacity of asexually reproduced A. psidii? Do different genetic groups of A. psidii represent cryptic species? What is the source of the Eucalypt/rose apple-brazil/uruguay biotype of A. psidii? What is the source of the Pandemic biotype of A. psidii?

35 Thank you! From: A.C. Alfenas

36 Acknowledgments

The threat of myrtle rust to Māori taonga plant species in New Zealand

The threat of myrtle rust to Māori taonga plant species in New Zealand David Teulon, Theresa Alipia, Hone Ropata, Jenny Green, Suvi Viljanen- Rollinson, Matthew Cromey, Kieren Arthur, Robin MacDiarmid,