Unraveling the Mechanisms of Virus-Induced Symptom Development in Plants

Abstract

Plant viruses, as obligate intracellular parasites, induce significant changes in the cellular physiology of host cells to facilitate their multiplication. These alterations often lead to the development of symptoms that interfere with normal growth and development, causing USD 60 billion worth of losses per year, worldwide, in both agricultural and horticultural crops. However, existing literature often lacks a clear and concise presentation of the key information regarding the mechanisms underlying plant virus-induced symptoms. To address this, we conducted a comprehensive review to highlight the crucial interactions between plant viruses and host factors, discussing key genes that increase viral virulence and their roles in influencing cellular processes such as dysfunction of chloroplast proteins, hormone manipulation, reactive oxidative species accumulation, and cell cycle control, which are critical for symptom development. Moreover, we explore the alterations in host metabolism and gene expression that are associated with virus-induced symptoms. In addition, the influence of environmental factors on virus-induced symptom development is discussed. By integrating these various aspects, this review provides valuable insights into the complex mechanisms underlying virus-induced symptoms in plants, and emphasizes the urgency of addressing viral diseases to ensure sustainable agriculture and food production.

Keywords: cellular process; chloroplast; environmental factors; hormone; metabolome; plant virus; reactive oxidative species; transcriptome; virus-host interaction.

Figure 1

Key discoveries on the impact of plant viruses on cellular processes facilitating symptoms development through interactions with host proteins. Plant viruses disrupt various cellular functions by interacting with host proteins, including dysfunction of chloroplast proteins, hormone manipulation, accumulation of reactive oxygen species (ROS), and cell cycle control, which contribute to the development of different types of symptoms. PSbO, Photosystem II oxygen-evolving complex protein; PSbP, luminal protein complex associated with photosystem II; Fd I, chloroplast ferredoxin I; MinD, chloroplast division-related factor; CHLI, chlorophyll biosynthesis gene; IAA10, a rice auxin/indole-3-acetic acid protein; PAP1, a putative regulator of auxin response genes; GAI: DELLA proteins; RBR: retinoblastoma-related proteins; SKη: glycogen synthase kinase; glycogen synthase kinase 3; CAT: catalase; CSD: Cu/Zu superoxide dismutase; PPDK: pyruvate orthophosphate dikinase; TGB3: triple gene block 3; SP: disease-specific protein; CP: coat protein; AltMV, Alternanthera mosaic virus; RSV, rice stripe virus; CMV, cucumber mosaic virus; PVY, potato virus Y; RDV, rice dwarf virus; TMV, tobacco mosaic virus; ALCScV, ageratum leaf curl Sichuan virus; WDV, wheat dwarf virus; FBNYV, faba bean necrotic yellow virus; TGMV, tomato golden mosaic virus; TLCYnV, tomato leaf curl Yunnan virus; MCMV, maize chlorotic mottle virus; BaMV, bamboo mosaic virus; SCMV, sugarcane mosaic virus.

Figure 2

The possible models of interactions among different cellular molecular functional pathways result in the manifestation of symptoms during viral infection. During virus infection in plant cells, the replication of the virus increases the energy demand, thus impacting energy metabolism. This leads to an upregulation of host respiratory metabolism and a downregulation of photosynthesis, resulting in elevated levels of reactive oxygen species (ROS). The high levels of ROS, as highly reactive molecules, can cause damage to cellular components, leading to symptoms such as chlorosis or necrosis. Furthermore, ROS can act as signaling molecules to regulate the synthesis and signal transduction of plant hormones. Altered hormone synthesis can hinder host development and photosynthesis, resulting in symptoms such as dwarfing and leaf curling. The impairment of chloroplast function and gene expression during viral infection contributes to symptoms such as chlorosis, mosaic, and yellowing.

Figure 3

Environmental factors that influence the development of viral symptoms include light and temperature. In general, there is a positive correlation between light intensity and the severity of viral symptoms. However, the correlation between temperature and viral symptoms can vary depending on the specific virus and host. For some viruses like tomato spotted wilt virus (TSWV), wheat streak mosaic virus (WSMV), and cucumber mosaic virus (CMV), higher temperatures are associated with enhanced symptoms development, indicating a positive correlation. On the other hand, certain viruses like potato virus Y (PVY), potato virus A (PVA), sweet potato chlorotic stunt virus + sweet potato feathery mottle virus (SPCSV + SPFMV), cassava brown streak virus + Ugandan cassava brown streak virus (CBSV + UCBSV), and alternanthera mosaic virus (AltMV) induced symptoms show a negative correlation with temperatures, where high temperatures inhibit the symptoms development.