Tumours induced by a plant virus are derived from vascular tissue and have multiple intercellular gateways that facilitate virus movement

Abstract

Structural studies showed that tumours induced by Southern rice black-streaked dwarf virus (SRBSDV; genus Fijivirus, family Reoviridae) were highly organized, modified phloem, composed of sclerenchyma, vessels, hyperplastic phloem parenchyma and sieve elements (SEs). Only parenchyma and SEs were invaded by the virus. There was a special region that consisted exclusively of SEs without the usual companion cells and a new flexible type of intercellular gateway was observed on all SE-SE interfaces in this region. These flexible gateways significantly increased the intercellular contacts and thus enhanced potential symplastic transport in the tumour. Flexible gateways were structurally similar to compressed plasmodesmata but were able to accommodate complete SRBSDV virions (~80 nm diameter). Virions were also found in sieve-pore gateways, providing strong evidence for the movement of a virus with large virions within phloem tissue and suggesting that the unusual neovascularization of plant virus-induced tumours facilitated virus spread. A working model for the spread of tumour-inducing reoviruses in plants is presented.

Biology of Southern rice black‐streaked dwarf virus: a novel fijivirus emerging in East Asia

“…a), making them larger than most plant viruses. Negative staining reveals a smooth inner core (50–55 nm in diameter) without spikes, an outer core with tower‐like B‐spikes, and a double‐layer with both B‐ and A‐spikes (75–80 nm in diameter) (Xie et al ., ). In the cytoplasm of phloem parenchyma cells in infected hosts, large quantities of viral particles form crystalline arrays (Fig.…”

“…Thus the phloem part of the vascular bundle of rice stems proliferates to form a tumour protrusion after SRBSDV infection. This tumour is full of abnormal sieve elements (SE) and phloem parenchyma cells but without conventional companion cells, and large amounts of virus particles accumulate in this tissue (Xie et al ., ). Viral gene expression is more active in tumours than in other tissues (He et al ., ).…”

“…Viral gene expression is more active in tumours than in other tissues (He et al ., ). Examination of the cellular interfaces of SEs in tumours shows not only sieve pores but a novel specific intercellular gateway that appears small but may contain large virus particles (80 nm), and this perhaps represents a new pattern of plasmodesma (PD) modification (Xie et al ., ). Tumorigenesis may be associated with interactions between viral proteins and cellular factors to interfere with the host cell cycle.…”

“…Having been delivered by viruliferous WBPH to a previously healthy plant, a new cycle in the host plant is initiated. SRBSDV is limited to SEs and phloem parenchyma (Xie et al ., ), where large amounts of virions and viroplasms accumulate. A recent report shows that the hyperplastic phloem parenchyma within the SRBSDV‐induced tumours serve as the main sites for viral propagation and virion assembly and that the hyperplastic SEs of the tumours facilitate virus movement (Xie et al ., ).…”

“…SRBSDV is limited to SEs and phloem parenchyma (Xie et al ., ), where large amounts of virions and viroplasms accumulate. A recent report shows that the hyperplastic phloem parenchyma within the SRBSDV‐induced tumours serve as the main sites for viral propagation and virion assembly and that the hyperplastic SEs of the tumours facilitate virus movement (Xie et al ., ). The virus does not appear to invade seeds or be transmitted by seeds (Pu et al ., ).…”