Integrated epidemiology, viral genomics and molecular host response mechanisms to sweet potato viruses

Abstract

Sweetpotato (Ipomoea batatas L.) is a critical food security and income crop in subSaharan Africa (SSA), especially for smallholder farmers, but its production faces severe constraints from Sweetpotato virus disease (SPVD), resulting from synergistic co-infection by Sweet potato feathery mottle virus (SPFMV) and Sweet potato chlorotic stunt virus (SPCSV), leading to yield losses of up to 98%. This study examined the epidemiology, genetic diversity and host resistance mechanisms of SPVD in Uganda through a multi-faceted approach. A socio-economic and disease survey of 95 households/fields across central (n=33), eastern (n=30), and western (n=32) regions revealed widespread SPVD incidence (up to 100% in some areas), with farmers identifying it as the primary constraint, yet nearly half lacked knowledge of symptoms, vectors (aphids and whiteflies), and management practices; adoption of controls like rogueing and clean planting material was low, influenced positively by education and symptom awareness but negatively by farming experience and land size, highlighting needs for gender-sensitive training and extension services. Next-generation sequencing (NGS) of diseased vines from 48 samples identified nine viruses, including first reports of Sweetpotato pakakuy virus (SPPV) and Sweetpotato symptomless virus-1 (SPSMV1) in Uganda, with frequent mixed infections; phylogenetic and recombination analyses showed high diversity in SPFMV and Sweetpotato virus C (SPVC), driven by mutations, recombination events (especially in coat protein and helper component proteinase genes), and purifying/diversifying selection, affirming East Africa as a viral evolution hotspot. An experimental transcriptomic study of three cultivars ('Beauregard' as susceptible, 'Tanzania' as moderately tolerant, and 'New Kawogo' as highly tolerant) infected with SPFMV, SPCSV, or SPVD at 3-, 6-, and 12-weeks postinoculation. Transcriptomic profiling uncovered cultivar-specific responses: 'New Kawogo' demonstrated robust resistance via early upregulation of redox regulation, transcriptional factors, hormonal signaling (e.g., salicylic acid and systemic acquired resistance), and detoxification, enabling full recovery; 'Tanzania' exhibited adaptive, delayed immune activation with partial tolerance through metabolic reprogramming and MAPK pathways; while 'Beauregard' showed susceptibility marked by transcriptional repression, immune suppression, and failure to recover. These results underscore knowledge gaps, viral diversity, and differential host defenses as key factors in SPVD persistence, providing candidate genes (e.g., oxidoreductases, ATP-binding proteins, SUMOylation regulators) for marker-assisted breeding and functional genomics to develop resilient varieties, ultimately enhancing sustainable sweetpotato production, food security, and livelihoods in SSA.