Phytophthora: an ancient, historic, biologically and structurally cohesive and evolutionarily successful generic concept in need of preservation

Abstract

The considerable economic and social impact of the oomycete genus Phytophthora is well known. In response to evidence that all downy mildews (DMs) reside phylogenetically within Phytophthora, rendering Phytophthora paraphyletic, a proposal has been made to split the genus into multiple new genera. We have reviewed the status of the genus and its relationship to the DMs. Despite a substantial increase in the number of described species and improvements in molecular phylogeny the Phytophthora clade structure has remained stable since first demonstrated in 2000. Currently some 200 species are distributed across twelve major clades in a relatively tight monophyletic cluster. In our assessment of 196 species for twenty morphological and behavioural criteria the clades show good biological cohesion. Saprotrophy, necrotrophy and hemi-biotrophy of woody and non-woody roots, stems and foliage occurs across the clades. Phylogenetically less related clades often show strong phenotypic and behavioural similarities and no one clade or group of clades shows the synapomorphies that might justify a unique generic status. We propose the clades arose from the migration and worldwide radiation ~ 140 Mya (million years ago) of an ancestral Gondwanan Phytophthora population, resulting in geographic isolation and clade divergence through drift on the diverging continents combined with adaptation to local hosts, climatic zones and habitats. The extraordinary flexibility of the genus may account for its global 'success'. The 20 genera of the obligately biotrophic, angiosperm-foliage specialised DMs evolved from Phytophthora at least twice via convergent evolution, making the DMs as a group polyphyletic and Phytophthora paraphyletic in cladistic terms. The long phylogenetic branches of the DMs indicate this occurred rather rapidly, via paraphyletic evolutionary 'jumps'. Such paraphyly is common in successful organisms. The proposal to divide Phytophthora appears more a device to address the issue of the convergent evolution of the DMs than the structure of Phytophthora per se. We consider it non-Darwinian, putting the emphasis on the emergent groups (the DMs) rather than the progenitor (Phytophthora) and ignoring the evolutionary processes that gave rise to the divergence. Further, the generic concept currently applied to the DMs is narrower than that between some closely related Phytophthora species. Considering the biological and structural cohesion of Phytophthora, its historic and social impacts and its importance in scientific communication and biosecurity protocol, we recommend that the current broad generic concept is retained by the scientific community.

Keywords: Biosecurity; Cladism; Downy mildews; Economic impact; Molecular phylogeny; Oomycetes; Paraphyly.

Fig. 1

Number of described and accepted Phytophthora species over time. Adapted from Brasier (2009). Data from pre-molecular era publications (Tucker ; Waterhouse ; Stamps et al. ; Erwin and Ribeiro 1996) include only those species currently accepted as valid species

Fig. 2

Number of important Phytophthora declines and diebacks of forests and natural ecosystems over time. Adapted from Jung et al. (2018a). [1 = ink disease of Castanea sativa in Europe (observation of first typical symptoms in 1838), 2 = ink disease of Castanea dentata in the USA (observation of first typical symptoms in 1824), 3 = decline of Fagus sylvatica in the UK, 4 = littleleaf disease of pines in the USA, 5 = decline and mortality of Chamaecyparis lawsoniana in the Pacific Northwest, 6 = jarrah dieback in Western Australia (WA; observation of first typical symptoms in the 1920s), 7 = ink disease of C. crenata and chestnut hybrids in Korea, 8 = eucalypt dieback in Victoria (observation of first typical symptoms in 1935), 9 = kauri dieback in New Zealand, 10 = Dieback of Nothofagus forests in Papua New Guinea, 11 = Mediterranean oak decline, 12 = Alnus mortality in Europe, 13 = temperate European oak decline, 14 = decline of F. sylvatica in mainland Europe, 15 = Sudden Oak Death in California and Oregon, 16 = littleleaf disease of Pinus occidentalis in the Dominican Republic, 17 = mortality of Austrocedrus chilensis in Argentina (observation of first typical symptoms in 1948), 18 = leaf and shoot blight of eucalypt plantations in New Zealand, 19 = oak decline in the Eastern USA, 20 = root and collar rot of eucalypt plantations in South Africa, 21 = needle cast and defoliation of Pinus radiata in Chile, 22 = dieback of Eucalyptus gomphocephala in WA, 23 = dieback of riparian Eucalyptus rudis in WA, 24 = Sudden Larch Death in the UK, 25 = dieback of Araucaria excelsa in Brazil, 26 = Ash decline in Denmark and Poland, 27 = dieback of Nothofagus spp. in the UK, 28 = mortality of Juniperus communis in the UK, 29 = red needle cast of P. radiata in New Zealand, 30 = leaf and twig blight of Ilex aquifolium in Corsica and Sardinia, 31 = dieback of Mediterranean maquis vegetation, 32 = Dieback of Fagaceae-Lauraceae monsoon forests in Northern Taiwan, 33 = Dieback of subtropical Fagaceae forests in Southern Taiwan, 34 = poplar dieback in Serbia, 35 = dieback of Valdivian rainforests in Chile, 36 = gummosis of Acacia mearnsii plantations in Brazil, 37 = collar rot of P. radiata plantations in New Zealand, 38 = dieback of laurosilva cloud forests in Northern Vietnam, 39 = black butt of Acacia mangium plantations in Vietnam, 40 = decline of Cinnamomum cassia plantations in Vietnam, 41 = cankers and dieback of Western hemlock and Douglas fir in the UK.]

Fig. 3

Phylogenetic tree of the Phytophthora clades and representative downy mildews. Redrawn from Scanu et al. (2021). A fifty percent majority rule consensus phylogram derived from maximum likelihood analysis of a concatenated four-locus (ITS, Btub, cox1, nadh1) dataset of representative species from phylogenetic Clades 1–12 of Phytophthora and the four downy mildew groups DMPH, DMCC, GDM, and BDM. Maximum likelihood bootstrap values and Bayesian posterior probabilities are indicated but not shown below 60% and 0.80, respectively. Nothophytophthora amphigynosa was used as outgroup taxon (not shown). Scale bar = 0.01 expected changes per site per branch

Fig. 4

Breeding systems, main morphological characters and cardinal temperatures for growth of 196 culturable species in the 11 major Phytophthora clades and the genus showing percentage of species per clade or genus

Fig. 5

Lifestyles, diseases and host ranges of 196 culturable species in the 11 major Phytophthora clades and the genus showing percentage of species per clade or genus