Tobacco Mosaic Virus Infection Results in an Increase in Recombination Frequency and Resistance to Viral, Bacterial, and Fungal Pathogens in the Progeny of Infected Tobacco Plants      

Abstract

Our previous experiments showed that infection of tobacco (Nicotiana tabacum) plants with Tobacco mosaic virus (TMV) leads to an increase in homologous recombination frequency (HRF). The progeny of infected plants also had an increased rate of rearrangements in resistance gene-like loci. Here, we report that tobacco plants infected with TMV exhibited an increase in HRF in two consecutive generations. Analysis of global genome methylation showed the hypermethylated genome in both generations of plants, whereas analysis of methylation via 5-methyl cytosine antibodies demonstrated both hypomethylation and hypermethylation. Analysis of the response of the progeny of infected plants to TMV, Pseudomonas syringae, or Phytophthora nicotianae revealed a significant delay in symptom development. Infection of these plants with TMV or P. syringae showed higher levels of induction of PATHOGENESIS-RELATED GENE1 gene expression and higher levels of callose deposition. Our experiments suggest that viral infection triggers specific changes in progeny that promote higher levels of HRF at the transgene and higher resistance to stress as compared with the progeny of unstressed plants. However, data reported in these studies do not establish evidence of a link between recombination frequency and stress resistance.

Changes in homologous recombination frequency in Arabidopsis thaliana plants exposed to stress depend on time of exposure during development and on duration of stress exposure

“…The progeny of plants exposed to various heavy metal salts had longer roots if grown under non-induced conditions or exposed to heavy metal salts over again (Rahavi et al 2011). The progeny of tobacco plants infected with oilseed rape mosaic virus was larger in size and tolerated stress better than the progeny of non-stressed plants (Kathiria, et al 2010). The progeny of infected tobacco plants also appeared to accumulate more metabolites, especially sugars and amino acids, as compared to the progeny of control plants (Mandal et al 2012).…”

“…Various stresses were shown to alter HRF in the progeny, including exposures to UV-C, temperature changes, salt and paraquat as well as infection with pathogens (Boyko et al 2010a;Kathiria et al 2010;Molinier et al 2006;Pecinka et al 2009). The majority of these stresses were applied to plants at a young age (7 dpg), although several of them were applied at 12 dpg or later (Pecinka et al 2009).…”

“…In several recent publications, it has been demonstrated that the progeny of stressed plants can better cope with similar and different stresses (Boyko et al 2010a, b;Kathiria et al 2010;Luna et al 2012;Rasmann et al 2012;Slaughter et al 2012). Transgenerational memory has an epigenetic component, and it likely depends on the activity of small interfering RNAs, differential patterns of DNA methylation and histone modification in gametes and embryos (Boyko et al 2007;Boyko and Kovalchuk 2011;Ito et al 2011;Mirouze and Paszkowski 2011).…”

“…Many stresses were shown to alter the frequency of somatic homologous recombination (HRF), including gamma-and Xrays, exposures to UV-C and UV-B, treatments with chemicals causing oxidative stress, herbicides as well as changes in temperature and water regimes and infection with pathogens (Besplug et al 2004;Boyko et al 2005Boyko et al , 2010aFilkowski et al 2004;Kathiria et al 2010;Kovalchuk et al 2000;Lucht et al 2002;Molinier et al 2005;Pecinka et al 2009;Ries et al 2000;Yao and Kovalchuk 2011). The influence of stress on the frequency of homologous recombination cannot be underestimated since HR is able to rearrange the plant genome substantially, thus leading to loss of heterozygocity.…”

“…Exposure to stress is also known to influence the frequency of meiotic recombination (Kovalchuk et al 2003;Ries et al 2000). Moreover, several experiments showed that the progeny of stressed plants exhibited higher levels of somatic HRF without being exposed to any stress (Boyko et al 2007(Boyko et al , 2010a; Kathiria et al 2010;Molinier et al 2006;Pecinka et al 2009).…”