Musa Germplasm A and B Genomic Composition Differentially Affects Their Susceptibility to Banana Bunchy Top Virus and Its Aphid Vector, Pentalonia nigronervosa

Abstract

Banana bunchy top disease (BBTD), caused by the banana bunchy top virus (BBTV, genus Babuvirus), is the most destructive viral disease of banana and plantain (Musa spp.). The virus is transmitted persistently by the banana aphid, Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae). While research efforts have focused on screening Musa genotypes for BBTD resistance, comparatively little work has been carried out to identify resistance to banana aphids. This study assessed 44 Musa germplasm of different A and B genome composition for the performance of banana aphids under semicontrolled environmental screenhouse conditions and in a field trial established in a BBTD endemic location. In the screenhouse, the AA diploid Calcutta 4 had the lowest apterous aphid density per plant (9.7 ± 4.6) compared with AAB triploid Waema, which had the highest aphid densities (395.6 ± 20.8). In the field, the highest apterous aphid density per plant (29.2 ± 6.7) occurred on the AAB triploid Batard and the lowest (0.4 ± 0.2) on the AA diploid Pisang Tongat. The AA diploid Tapo was highly susceptible to BBTD (100% infection) compared with the genotypes Balonkawe (ABB), PITA 21 (AAB), Calcutta 4 (AA), and Balbisiana Los Banos (BB), which remained uninfected. The Musa genotypes with apparent resistance to BBTD and least susceptibility to aphid population growth provide options for considering aphid and BBTD resistance in banana and plantain breeding programs.

The aphidPentalonia nigronervosa(Hemiptera: Aphididae) takes advantage from the quality change in banana plant associated withBanana bunchy top virusinfection

“…Furthermore, the higher fecundity per aphid age, as well as the higher total fecundity per female (Ro), on plantain compared with dessert banana (irrespective of infection status) is thought to be due to the difference in internal resource composition between Cavendish (strict triploid—AAA) and Pacific plantain (triploid hybrid—AAB) genotypes, in particular to the ratio of carbohydrates to amino acids in the phloem (Simmonds 1962, Mauck et al 2014). This is consistent with the recent study of Ngatat et al (2022), who evaluated 44 Musa germplasm plants of different genetic compositions A and B for their performance against banana aphids. In general, dessert banana plants had the lowest aphid density per plant compared with plantain banana plants.…”

“…Daily fecundity per female varied with both virus infection and genotype, with stronger dynamics for infected plantain banana plant than for other banana types (healthy dessert banana, infected dessert banana, and healthy plantain banana plants), and lower for healthy dessert banana plant than for other banana types (infected dessert banana, healthy plantain banana, and infected plantain banana plants). Dessert banana plants are very susceptible to many diseases due to their narrow genetic base (Abadie et al 2003, Ngatat et al 2022). This is consistent with previous studies where aphids reared on infected plants produced higher numbers of nymphs than aphids reared on healthy plants (Colvin et al 2006, Bosque-Pérez and Eigenbrode 2011, Eigenbrode et al 2018).…”

“…Pentalonia nigronervosa established and multiplied more rapidly on plantain plants, which are a wilder genotype (Simmonds 1962) and therefore less susceptible to BBTV, compared with Cavendish dessert bananas (severely damaged by BBTV), highly domesticated and known to be highly susceptible to BBTV (Su et al 1992, Hooks et al 2008, 2009, Ngatat et al 2022). We therefore suggest that BBTV infection excessively deteriorates the dessert banana, to the extent that it is of poor quality for P. nigronervosa in terms of survival rate and longevity of the aphids that colonize it.…”

Distribution and diversity of emergent Banana bunchy top virus infecting banana and plantain in Cameroon, Central Africa

“…It is well known that crop monocultures of homogeneous genetic backgrounds are more susceptible to severe disease outbreaks than crop mixtures (Garrett & Mundt, 1999). In the BBTD‐affected South region of Cameroon, banana cultivation is a variety mixture predominantly of AAB local plantains (Table S1), which are moderately susceptible to BBTD with a variable rate of spread, as shown in two trials organized in different locations in the South of Cameroon (Ngatat et al., 2017, 2022). Banana crop land connectivity risk indexing based on network modelling has suggested influence of several factors, including agroecology, cultivars and crop management practices on rate of pathogen spread in a geographic region (Xing et al., 2020).…”

Comparative RNA-seq analysis of resistant and susceptible banana genotypes reveals molecular mechanisms in response toBanana bunchy top virus(BBTV)

“…Still, utilizing natural sources of resistance in breeding programs is still far the most effective and longterm strategy to combat its negative impact on the banana industry. Cultivated banana types, such as 'Cavendish' and 'Lakatan' varieties, are susceptible to BBTV 6,55 , unlike the wild type banana progenitor M. balbisiana which exhibits resistance to the disease 56 . In recent years, the progress of next-generation sequencing and bioinformatics approaches, such as transcriptome-wide expression studies using RNA-seq data, has been heavily utilized in the study of plant-pathogen interactions.…”