Cassava Frogskin Disease: Current Knowledge on a Re-Emerging Disease in the Americas

Abstract

Cassava frogskin disease (CFSD) is a graft-transmissible disease of cassava reported for the first time in the 1970s, in Colombia. The disease is characterized by the formation of longitudinal lip-like fissures on the peel of the cassava storage roots and a progressive reduction in fresh weight and starch content. Since its first report, different pathogens have been identified in CFSD-affected plants and improved sequencing technologies have unraveled complex mixed infections building up in plants with severe root symptoms. The re-emergence of the disease in Colombia during 2019-2020 is again threatening the food security of low-income farmers and the growing local cassava starch industry. Here, we review some results obtained over several years of CFSD pathology research at CIAT, and provide insights on the biology of the disease coming from works on symptoms' characterization, associated pathogens, means of transmission, carbohydrate accumulation, and management. We expect this work will contribute to a better understanding of the disease, which will reflect on lowering its impact in the Americas and minimize the risk of its spread elsewhere.

Keywords: cassava; cassava frogskin disease; root yield; storage root; sugar content.

Figure 1

Root symptoms of CFSD as observed in four different field-infected cassava genotypes: Valencia, BRA383, Reina (CM6740-7), and Secundina (MCOL2063). Top pictures correspond to roots showing no symptoms of the disease. Bottom pictures show the characteristic root symptoms of CFSD.

Figure 2

A timeline of the main results on the search for the causal agent of CFSD. Pineda et al., 1983 [1], Pineda et al., 1980 [7]; Pineda et al., 1981 [8]; Cuervo 1990 [9]; Nolt et al., 1992 [10]; Roa et al., 2000 [11]; Chaparro-Martinez and Trujillo-Pinto, 2001 [12]; Alvarez et al., 2009 [13]; Calvert et al., 2008 [14]; Carvajal et al., 2014 [15]; de Oliveira et al., 2014 [16]; de Souza et al., 2014 [17]; Cardozo et al., 2016 [18]; de Oliveira et al., 2020 [19].

Figure 3

Map showing the current geographical distribution of CFSD according to a global literature search using Google Scholar, using search terms ‘mandioca couro de sapo’, ‘yuca cuero de sapo’, and ‘cassava frogskin’. Information from internal CIAT annual reports is included. The interactive map and links to the historical reports are available at: https://pestdisplace.org/embed/news/map/disease/5 [28]. The information was last accessed on 20 April 2022.

Figure 4

Sugar content in four different genotypes from Costa Rica (Valencia and Señorita) and Colombia (Bra383 and Reina). Dry matter was expressed as the percentage of dry weight relative to fresh weight. Sugar (and organic acids) analysis was carried out from a 500 mg flour sample. Two determinations were carried out with each flour sample. Sugars were analyzed using HPLC (Agilent Technologies 1200 series, Waldbronn, Germany). Samples were separated isocratically at 0.6 mL/min and at 30 °C and retention times and standard curves were prepared for glucose (Sigma-Aldrich, St. Louis, MO, USA, G7528), fructose (Sigma-Aldrich F2543), and saccharose (Sigma-Aldrich; ≥99.5%; S7903). p-values < 0.05 (*) were considered as significant. Error bars are the mean +/− SEM (standard error of the mean).

Figure 5

Phytoplasmas detected in CFSD-affected plants belong to the 16Sr ribosomal group III (in red). Restriction analysis (left) of the 16S RNA region amplified by nested PCR. Phylogenetic analysis of the 16Sr sequences of phytoplasmas isolated from cassava (right) in the Americas (in red) and Southeast Asia. L = Ladder. CWBD = cassava witches’ broom disease. L = DNA Ladder (Bioline, USA). The asterisks indicates the 300 bp band.

Figure 6

Distinct patterns of dsRNA detected in cassava plants affected by CSFD. Cuervo reported at least two dsRNA patterns in plants with CFSD [10]. Both patterns show 10 dsRNA bands. Left: Patterns P1 and P2 can be detected in samples from the Amazon region of Colombia. P2 is more common in samples from other regions (photo kindly provided by M. Cuervo). NI = Not infected control. L = 1 kb ladder. The asterisks indicates the 2 kb band. Right: Phylogenetic analysis of reovirids infecting plants based on the amino acid sequence of the RdRp domain. RRSV = Rice ragged stunt virus (NC_003771); RpLV = Raspberry latent virus (NC_014600); FDS = Fiji disease virus (NC 007159); MRCV = Mal de Rio Cuarto virus (NC 008733); RBSDV = Rice black-streaked dwarf virus (HM585279); MRDV = Maize rough dwarf virus (KU984966); RDV = Rice dwarf virus (NC 003773); RGVD = Rice gall dwarf virus (NC_009248); GCSV = Grapevine Cabernet Sauvignon reovirus (KM378723).