Detection of aroid leaf rust Pseudocerradoa paullula on Swiss cheese plant Monstera deliciosa in the continental USA.

Abstract

Monstera deliciosa Liebm. (Araceae, Monocots), sometimes referred to as Swiss cheese plant, is one of the most common aroids used as an indoor and landscape ornamental plant (Cedeño et al. 2020). Production of M. deliciosa and other closely related Araceae species represents an important sector of the ornamental nursery business worldwide. Swiss cheese plant is believed to have originated in the tropical forests of southern Mexico, where its fruit is considered a delicacy due to its sweet, exotic flavor (Cedeño et al. 2020). Since 2019, symptomatic Monstera plants from two plant nurseries and residential properties in South Florida were submitted for disease diagnosis to the Florida Department of Agriculture and Consumer Services, Division of Plant Industry (FDACS-DPI) in Gainesville, Florida, and to the University of Florida, Tropical Research and Education Center Plant Clinic in Homestead, Florida. Symptoms included small chlorotic spots on the leaf surface, which expanded and became brown to reddish-brown often with a yellow halo and produced uredinia with abundant urediniospores. The pathogen was identified morphologically as the rust fungus Pseudocerradoa (=Puccinia) paullula (Syd. & P. Syd.) M. Ebinghaus & Dianese (Pucciniaceae, Basidiomycota) (Ebinghaus et al. 2022), characterized by the production of pseudosuprastomatal uredinia. Uredinospores light-brown and globose, echinulate (1 µm height), reddish to light brown, 24 - 31 µm diameter, with thick walls, 1.5 - 2.5 µm height (n=15). Teliospores 2-celled, light-yellow and ellipsoidal, 23 - 28 × 19 - 24 µm (n =15) were observed in sori appearing as dark-brown leaf spots on the adaxial side of the leaves (e-Xtra Fig. 1). Molecular characterization of the fungal pathogen was based on the small subunit (SSU), internal transcribed spacer (ITS), and large subunit (LSU) of the ribosomal RNA genes (Aime 2006) with the addition of a LSU internal primer specific for the rust species Ppaullula_int-forward 5'ATAGTTATTGGCTTTGATTTACA-3' designed in this study to increase the quality and the sequence read length due to a 3'- ~21-Ts-homopolymer (e-Xtra Fig. 2) (GenBank accession number ON887196, ON887197, OQ275200, OQ275201). In addition to morphological identification, the host plant was identified using the Ribulose-1,5-bisphosphate carboxylase-oxygenase (rbcL) and Maturase K (matK) genes (Fazekas et al. 2012) (GenBank accession numbers ON887189, ON887193, respectively). MegaBlast searches confirmed the morphological identification with 100% identity to M. deliciosa vouchers GQ436772 and MK206496, respectively (Chen et al. 2015). Dried specimens were deposited in the Plant Industry Herbarium Gainesville (PIHG 16226, 16227, 17154, 17155). Molecular identification of the rust pathogen P. paullula was carried out through megaBlast (Chen et al. 2015) searches together with a phylogenetic analysis performed in RAxML v8 (Stamatakis 2014) (e-Xtra Fig. 3). Koch's postulates were performed by using urediniospores, collected from an infected sample and were kept for 7 days at 4 C, as an inoculum source. Healthy rooted M. deliciosa plants were inoculated by rubbing the inoculum on both leaf surfaces at >90% RH, room temperature, 12/12 light cycle. After the incubation period (48 h), plants were placed in a climate-controlled greenhouse and watered twice a week, ~30 C, ~65 RH, 12/12 light cycle. After three weeks, all inoculated plants developed symptoms resembling those observed on the samples submitted for disease diagnosis. Controls did not show symptoms. Spores from the pustules of inoculated plants were identified as P. paullula by both morphology and molecular means. The genus Pseudocerradoa comprises P. paullula and its sister species P. rhaphidophorae (Syd.) M. Ebinghaus & Dianese. Both species can be distinguished by size and coloration of urediniospores and their host range within the Araceae. Pseudocerradoa rhaphidophorae produces smaller urediniospores and only occurs on Rhaphidophora species (Shaw 1995). Pseudocerradoa paullula is not considered fully established in Florida, since the host distribution is mainly restricted to indoors and M. deliciosa is rarely used as an outdoor ornamental (Wunderlin et al. 2023). Here we name the disease caused by P. paullula as "aroid leaf rust", due to its ability to infect several species in this plant family. Other closely related hosts reported as susceptible to this pathogen are Monstera standleyana G.S.Bunting (as M.s. cv. variegata), Monstera adansonii var. laniata (Schott) Mayo & I.M. Andrade, Monstera subpinnata (Schott) Engl., Typhonodorum lindleyanum Schott, and Stenospermation sp. (Shaw 1991, 1992, 1995). To date, the aroid leaf rust was only known from Australia, China, Japan, Malaysia, and Philippines (Lee et al. 2012; Shaw 1991). Based on our review, P. paullulla was intercepted once from Malaysia in 2014 at the port of Los Angeles, USA (BPI voucher 893085). This present study reports the establishment of P. paullula in Florida, USA infecting M. deliciosa.