Under siege: virus control in plant meristems and progeny

Abstract

In the arms race between plants and viruses, two frontiers have been utilized for decades to combat viral infections in agriculture. First, many pathogenic viruses are excluded from plant meristems, which allows the regeneration of virus-free plant material by tissue culture. Second, vertical transmission of viruses to the host progeny is often inefficient, thereby reducing the danger of viral transmission through seeds. Numerous reports point to the existence of tightly linked meristematic and transgenerational antiviral barriers that remain poorly understood. In this review, we summarize the current understanding of the molecular mechanisms that exclude viruses from plant stem cells and progeny. We also discuss the evidence connecting viral invasion of meristematic cells and the ability of plants to recover from acute infections. Research spanning decades performed on a variety of virus/host combinations has made clear that, beside morphological barriers, RNA interference (RNAi) plays a crucial role in preventing-or allowing-meristem invasion and vertical transmission. How a virus interacts with plant RNAi pathways in the meristem has profound effects on its symptomatology, persistence, replication rates, and, ultimately, entry into the host progeny.

Figure 1

Levels of control over vertical transmission of viruses/viroids. Many pathogenic viruses invade the entire plant body but most cannot enter shoot apical meristems, gametophytes, gametes, and/or embryos/seeds. Experimental data and agricultural practice suggest the existence of meristematic and transgenerational antiviral protection systems that prevent vertical transmission to progeny. How these defense mechanisms work, and the conditions under which some viruses can bypass the barriers, remains poorly understood.

Figure 2

Schematic representation of experimentally observed virus/viroid distribution in relation to the SAM. Virus-infected tissues are colored in violet. The virus is excluded from (A) the meristem dome (Sunpapao et al., 2009), (B) the entire SAM (e.g. WClMV [Foster et al., 2002]; PSTVd [Di Serio et al., 2010]), or (C) the entire apex except the vasculature (e.g. BDMV [Sudarshana et al., 1998]). D, The virus invades the SAM, including the outer layers of the meristem dome and leaf/flower primordia (e.g. chrysanthemum chlorotic mottle viroid [Ebata et al., 2019]; AV-2 [Kawamura et al., 2014]).

Figure 3

Schematic representation of experimentally observed virus/viroid infection routes during plant sexual reproduction. Virus-infected tissues are colored in violet. A, The virus invades all reproductive organs and is transmitted to the next generation, resulting in vertical transmission. B, The virus invades the reproductive organs only partially, with various temporal and spatial distribution patterns, except gametes and/or embryos. This is not vertical transmission sensu stricto but mimics vertical transmission to the seedling by post-germination mechanical inoculation of virions from the seed coat. C, A virus-infected pollen grain fertilizes a healthy plant and transmits infection to the mother plant (horizontal transmission) and/or the progeny (vertical transmission). Vertical transmission mechanisms proposed here were extrapolated from the following papers: (A) (Amari et al., 2007; Amari et al., 2009; Matsushita and Tsuda, 2014); (B) (Matsushita et al., 2011); (C) (Matsushita and Yanagisawa, 2018; Matsushita et al., 2018).

Figure 4

Schematic representation of recovery in connection to meristem invasion. Virus-infected tissues are colored in violet. A, In certain virus–host combinations, newly emerging organs from a systemically infected plant with strong disease symptoms show light or no symptoms, indicating recovery. Recovered tissues (colored in violet stripes) are resistant to super infection by viruses containing RNA sequences homologous to the originally infecting virus. Recovery and cross-protection can be related to meristem entry of the initial virus. B, During early stages of infection, nepoviruses predominantly invade the vasculature of the main stem, the leaf primordia, and the meristem dome (left). Later during recovery (right), the virus appears restricted to the meristem dome (Dong et al., 2009; Santovito et al., 2014). C, During early stages of infection, for example with TRV, the virus invades the SAM (left), but is later excluded from this tissue (right) (Martín-Hernández and Baulcombe, 2008).

Figure 5

Control by host- and virus-encoded factors over virus meristem invasion, vertical transmission, and recovery from acute infection. Virus-infected tissues and viral proteins/factors are colored in violet, host plant-encoded proteins are shown in green. Virus invasion of the SAM (bottom) can occur upon depletion of host proteins RDR6 and/or WUS, or due to virus-encoded proteins such as 16K (TRV), 2b (CMV), and TGB1 (WClMV). Weak/inefficient suppression of RNAi by viruses has also been suggested to allow viral SAM invasion. Virus invasion of the host progeny (top, left) resulting in vertical transmission has been linked to VSR proteins 12K (PEBV), HC-Pro (PSbMV), and γb (BSMV). Meristem invasion can also lead to recovery of newly emerging tissues from acute infection (top, right). Recovery has been linked to host antiviral RNAi factors including RDR6, and to VSR proteins 12K (PEBV), 2b (CMV), and 16K (TRV). Weak or inefficient suppression of RNAi by a virus can trigger both meristem invasion and recovery. A “recovered” state may in some instances correlate with high rates of vertical transmission.