First Report of Phytophthora heveae causing quick decline of macadamia in Hawai'i

Authors: Sugiyama, Lionel; HELLER, WADE - University Of Hawaii; BRILL, EVA - University Of Hawaii; Keith, Lisa

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/21/2020
Publication Date: 4/20/2020
Citation: Sugiyama, L.S., Heller, W., Brill, E., Keith, L.M. 2020. First Report of Phytophthora heveae causing quick decline of macadamia in Hawai'i. Plant Disease. 104(6):1875. https://doi.org/10.1094/PDIS-11-19-2451-PDN.
DOI: https://doi.org/10.1094/PDIS-11-19-2451-PDN

Interpretive Summary: Macadamia nut production in Hawaii is a $42.0 million industry. Macadamia quick decline (MQD), caused by Phytophthora tropicalis, has been a persistent problem in commercial macadamia production in Hawaii since 1986. Trees exhibiting symptoms of MQD were observed on Hawaii Island in 2016. This is the first report of P. heveae on macadamia and the first report of the pathogen on any host in Hawaii. Further work is needed to assess the full impact of P. heveae on macadamia in order to minimize tree loss in mature orchards and maintain the economic viability of Hawaii’s macadamia industry. Since P. heveae has a wider host range, our finding is also important because the presence of P. heveae in Hawaii poses a potential risk for avocado, mango and cacao production.

Technical Abstract: Macadamia (Macadamia integrifolia) nut production in Hawaii is a $42.0 million industry (USDA-NASS, 2019). Macadamia quick decline (MQD), caused by Phytophthora tropicalis, has been a persistent problem in commercial macadamia production in Hawaii since 1986; in the decades to follow thousands of trees have succumbed to MQD (Keith et al. 2010). The development of key diagnostic indicators and an innovative fungicide delivery method led to control of MQD (Keith et al. 2016). In October 2016, a macadamia tree exhibiting symptoms of MQD was observed at the USDA-ARS National Clonal Germplasm Repository in Hilo, Hawaii. Upon closer observation, a few younger branches exhibited slight wilting with curled, dull green leaves and sporadic browning of leaves occurred throughout the canopy. In addition, abundant dull, light green to chlorotic leaf litter with browning of petioles advancing partially in the leaf margins was present. Although some defoliation precedes tree death, MQD trees tend to retain most of their dead leaves. Discolored trunk tissue from the transition zone was plated onto amended water agar (Ko 1978) and within 7 days single hyphal tips were transferred to 10% V8 agar. Based on morphological characteristics (Erwin and Ribeiro 1996), isolate P16-45 was identified as P. heveae. The identification was confirmed using BLAST analysis of bulk sequenced PCR products of the ribosomal DNA ITS region, partial mitochondrial cytochrome oxidase subunit 1 (COX1) gene, partial mitochondrial NADH dehydrogenase subunit 1 (ND1) gene, and a partial enolase (ENL) gene (Kox et al. 2007; Weir et al. 2015; White 1990). Each gene sequence (GenBank accession nos. MN331558, MN331561, MN331564, and MN331567) was >99% identical to those of strain ICMP 19451, the ex-type culture of P. heveae. The TaqMan qPCR assay for Phytophthora spp. (Kox 2007) was used to initially screen additional island-wide trunk samples from trees exhibiting similar symptoms. Sequences of ITS, COX1, ND1, and ENL from isolates P16-52-1 (Holualoa, HI; November 2016) and P18-84 (North Kohala, HI; June 2018) were 100% identical to P16-45 (GenBank accession nos. MN331559-60, MN331562-63, MN331565-66, and MN331568-69). Pathogenicity tests were conducted on four macadamia saplings (mean height = 1.0 m) inoculated with sterile filter paper discs soaked in a 1.0 × 106 zoospore/ml suspension of P18-84 following the method of Keith et al. (2015). Two control plants were inoculated with sterile filter paper discs soaked in sterile water. Plants were maintained at 24°C with 12 h light in a growth chamber. The experiment was conducted twice. Six of 8 seedlings exhibited identical field symptoms within 4 to 8 weeks of inoculation. P. heveae was reisolated from all 6 plants and morphologically (10% V8 agar) and molecularly (ITS) identified, thus fulfilling Koch’s postulates. All control plants were asymptomatic and the fungus was not recovered on plates or detected by qPCR. P. heveae is not a common pathogen in North America. To the best of our knowledge, this is the first report of P. heveae on macadamia and the first report of the pathogen on any host in Hawaii. Further work is needed to assess the full impact of P. heveae on macadamia in order to minimize tree loss in mature orchards and maintain the economic viability of Hawaii’s macadamia industry. Since P. heveae has a wider host range, our finding is also important because the presence of P. heveae in Hawaii poses a potential risk for avocado, mango and cacao production.