Cassava mosaic geminiviruses: actual knowledge and perspectives

Abstract

SUMMARY Cassava mosaic disease (CMD) caused by cassava mosaic geminiviruses (CMGs) is one of the most devastating crop diseases and a major constraint for cassava cultivation. CMD has been reported only from the African continent and Indian subcontinent despite the large-scale cultivation of cassava in Latin America and several South-East Asian countries. Seven CMG species have been reported from Africa and two from the Indian subcontinent and, in addition, several strains have been recognized. Recombination and pseudo-recombination between CMGs give rise not only to different strains, but also to members of novel virus species with increased virulence and a new source of biodiversity, causing severe disease epidemics. CMGs are known to trigger gene silencing in plants and, in order to counteract this natural host defence, geminiviruses have evolved suppressor proteins. Temperature and other environmental factors can affect silencing and suppression, and thus modulate the symptoms. In the case of mixed infections of two or more CMGs, there is a possibility for a synergistic interaction as a result of the presence of differential and combinatorial suppressor proteins. In this article, we provide the status of recent research findings with regard to the CMD complex, present the molecular biology knowledge of CMGs with reference to other geminiviruses, and highlight the mechanisms by which CMGs have exploited nature to their advantage.

Figure 1

Geographical distribution of cassava‐infecting geminiviruses. Representatives of all species and strains of cassava mosaic geminiviruses (CMGs) in Africa and the Indian subcontinent. The green colour indicates the area under cassava cultivation and each different coloured dot represents a unique species. The virus name abbreviations are given in the text.

Figure 3

Recombination linearized map of representatives of the nine species of cassava‐infecting geminivirus and their strains. Each horizontal line represents the genotype of one virus isolate, and the different patterns and shades represent the tentative origins of the putative recombinant fragments. The length of the genome is indicated at the top of each diagram and the genome organization is depicted at the bottom; the abbreviated names of the virus isolates are listed on the left. The shades and patterns for the different original parental genome regions are provided below the genome organization. The numbers at the top of the diagram correspond to the length of the genome, starting at the nicking site of the conserved nona‐nucleotide TAATATT/AC. The virus name abbreviations are given in the text.

Figure 2

Genome organization of cassava mosaic geminiviruses (genus: Begomovirus). The genome is split into two components, termed DNA‐A (left) and DNA‐B (right). DNA‐A comprises six open reading frames (ORFs), and each ORF encodes a specific protein. AC1, replication‐associated protein (Rep); AC2, transcriptional activator protein (TrAP); AC3, replication enhancer protein (REn); AC4, RNA‐silencing suppressor; AV1, coat protein (CP); AV2, precoat protein. DNA‐B has two ORFs: BV1 encodes nuclear‐shuttle protein (NSP), and BC1 encodes movement protein (MP). C, Complementary‐sense ORFs; V, virion‐sense ORFs. The non‐coding intergenic region, also referred to as the common region (CR), with the stem‐loop structure is also depicted. The fragmented circles outside of the virus genome represent the DI‐DNAs of Indian cassava mosaic virus (ICMV) and Sri Lankan cassava mosaic virus (SLCMV) with their respective positions; dark and light grey lines represent DNA‐A and DNA‐B sequences, respectively. (Adapted from Patil et al., 2007.)

Figure 4

Sequence comparison of intergenic regions of cassava‐infecting begomoviruses depicting the iteron sequences and their relative positions. Comparison of DNA‐A components of representatives of all nine species and their strains, showing the location of iterons (highlighted with different shades for the different types of iteron) with reference to the TATA box and the stem‐loop with the nona‐nucleotide sequence embedded in it (boxed), and their orientation indicated by arrows, all located upstream of the stem‐loop structure. Spaces (‐) have been introduced to align the motifs, and each shade represents a unique iteron sequence. The virus name abbreviations are given in the text.

Figure 5

Differential virulence of cassava mosaic geminivirus (CMG) isolates. Symptoms of isolates of African cassava mosaic virus (ACMV) (top panels) and East African cassava mosaic virus—Uganda (EACMV‐UG) (bottom panels) reported from Uganda in 1998. Mild isolates and severe isolates are shown on the left and right, respectively.

Figure 6

Symptom severity of cassava plants. Dual infection leads to synergistic severe disease and corresponding post‐transcriptional gene silencing (PTGS) capacity of each virus. Second panel (from left to right): non‐infected healthy control plant; plant infected with African cassava mosaic virus (ACMV); plant infected with East African cassava mosaic Cameroon virus (EACMCV); dual infection with both viruses, which leads to synergistic severe disease (candle‐stick symptoms). The third panel indicates the function of AC2‐ and the bottom panel indicates the function of AC4‐type PTGS suppressor proteins. EACMCV‐AC2 (EAC2; third panel, second red image from right) and ACMV‐AC4 (AAC4; bottom panel, third red image from right) are positive for PTGS suppression. Synergism is explained by dual suppression of PTGS (red panels on the right). Green control panels (left) represent frame‐shift mutants of ACMV‐AC4 and EACMCV‐AC2 that have lost the capacity to suppress PTGS. ACMV‐AC2 is considered to be negative, as PTGS suppression is weak, and EACMCV‐AC4 is not a PTGS suppressor. (Adapted from Vanitharani et al., 2005.)