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Cereal crop production is severely affected by seed-borne bacterial diseases across the world. Locally occurring disease resistance in various crops remains elusive. Here, we have observed that rice plants of the same cultivar can be differentiated into disease-resistant and susceptible phenotypes under the same pathogen pressure. Following the identification of a seed-endophytic bacterium as the resistance-conferring agent, integration of high-throughput data, gene mutagenesis and molecular interaction assays facilitated the discovery of the underlying mode of action. Sphingomonas melonis that is accumulated and transmitted across generations in disease-resistant rice seeds confers resistance to disease-susceptible phenotypes by producing anthranilic acid. Without affecting cell growth, anthranilic acid interferes with the sigma factor RpoS of the seed-borne pathogen Burkholderia plantarii, probably leading to impairment of upstream cascades that are required for virulence factor biosynthesis. The overall findings highlight the hidden role of seed endophytes in the phytopathology paradigm of 'disease triangles', which encompass the plant, pathogens and environmental conditions. These insights are potentially exploitable for modern crop cultivation threatened by globally widespread bacterial diseases.

Since its domestication from wild rice thousands of years ago, rice has been cultivated largely through transplantation. During transplantation from the nursery to the paddy field, rice seedlings experience transplantation shock which affects their physiology and production. However, the mechanisms underlying transplantation shock and rice adaptation to this shock are largely unknown. Here, we isolated a transplant-sensitive chloroplast-deficient (tsc1) rice mutant that produces albino leaves after transplantation. Blocking light from reaching the juvenile leaves and leaf primordia caused chloroplast deficiencies in transplanted tsc1 seedlings. TSC1 encodes a noncanonical adenosine triphosphate-binding cassette (ABC) transporter homologous to AtNAP14 and is of cyanobacterial origin. We demonstrate that TSC1 controls plastid development in rice under dark conditions, and functions independently of light signaling. However, light rescued the tsc1 mutant phenotype in a spectrum-independent manner. TSC1 was upregulated following transplantation, and modulated the iron and copper levels, thereby regulating prolamellar body formation during the early P4 stage of leaf development. Therefore, TSC1 is indispensable for plastid development in the absence of light, and contributes to adaptation to transplantation shock. Our study provides insight into the regulation of plastid development and establishes a framework for improving recovery from transplantation shock in rice.

Accumulation of toxic heavy metals and metalloids (THMMs) in crop grain remarkably affects food safety and human health. Reducing the content of THMMs in grain requires the identification and manipulation of the genes regulating their accumulation. This study aimed to determine the genetic variations affecting grain THMM accumulation in rice by using association mapping. We used 276 accessions with 416 K single nucleotide polymorphisms (SNPs) and performed genome-wide association analysis of grain THMM concentrations in rice grown in heavily multi-contaminated farmlands. We detected 22, 17, and 21 quantitative trait loci (QTLs) for grain arsenic, cadmium, and lead concentrations, respectively. Both inter- and intra-subpopulation variants accounted for these QTLs. Most QTLs contained no known THMM-related genes and represented unidentified novel genes. We examined the candidate genes in qGAS1, a QTL for grain arsenic concentration with the best P-value detected for the entire population. We speculated that a transport protein of the multidrug and toxin extrusion family could be the candidate gene for this QTL. Our study suggested that the genetic regulation of grain THMM accumulation is very complex and largely unknown. The QTLs and SNPs identified in this study might help in the identification of new genes regulating THMM accumulation and aid in marker-assisted breeding of rice with low grain THMM content.

The sugar status of a plant acts as a signal affecting growth and development. The phenomenon by which high levels of sugars inhibit seedling establishment has been widely used to gain insight into sugar-signaling pathways. Natural allelic variation has been identified at the ANAC060 locus. The Arabidopsis Columbia ecotype produces a short ANAC060 protein without a transmembrane domain that is constitutively located to the nucleus, causing sugar insensitivity when overexpressed. In this study, we generated a genome-wide DNA-binding map of ANAC060 via chromatin immunoprecipitation sequencing using transgenic lines that express a functional ANAC060-GFP fusion protein in an anac060 background. A total of 3282 genes associated with ANAC060-binding sites were identified. These genes were enriched in biotic and abiotic stress responses, and the G-box binding motif was highly enriched in ANAC060-bound genomic regions. Expression microarray analysis resulted in the identification of 8350 genes whose activities were altered in the anac060 mutant and upon sugar treatment. Cluster analysis revealed that ANAC060 attenuates sugar-regulated gene expression. Direct target genes of ANAC060 included equivalent numbers of genes that were upregulated or downregulated by ANAC060. The various functions of these target genes indicate that ANAC060 has several functions. Our results demonstrate that ANAC060 directly binds to the promoter of ABI5 and represses the sugar-induced transcription of ABI5. Genetic data indicate that ABI5 is epistatic to ANAC060 in both sugar and abscisic acid responses.

Endogenous viral sequences in eukaryotic genomes, such as those derived from plant pararetroviruses (PRVs), can serve as genomic fossils to study viral macroevolution. Many aspects of viral evolutionary rates are heterogeneous, including substitution rate differences between genes. However, the evolutionary dynamics of this viral gene rate heterogeneity (GRH) have been rarely examined. Characterizing such GRH may help to elucidate viral adaptive evolution. In this study, based on robust phylogenetic analysis, we determined an ancient endogenous PRV group in Oryza genomes in the range of being 2.41-15.00 Myr old. We subsequently used this ancient endogenous PRV group and three younger groups to estimate the GRH of PRVs. Long-term substitution rates for the most conserved gene and a divergent gene were 2.69 x 10(-8) to 8.07 x 10(-8) and 4.72 x 10(-8) to 1.42 x 10(-7) substitutions/site/year, respectively. On the basis of a direct comparison, a long-term GRH of 1.83-fold was identified between these two genes, which is unexpectedly low and lower than the short-term GRH (>3.40-fold) of PRVs calculated using published data. The lower long-term GRH of PRVs was due to the slightly faster rate decay of divergent genes than of conserved genes during evolution. To the best of our knowledge, we quantified for the first time the long-term GRH of viral genes using paleovirological analyses, and proposed that the GRH of PRVs might be heterogeneous on time scales (time-dependent GRH). Our findings provide special insights into viral gene macroevolution and should encourage a more detailed examination of the viral GRH.

Supporting information : http://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1006413#sec015, The interplay of different virus species in a host cell after infection can affect the adaptation of each virus. Endogenous viral elements, such as endogenous pararetroviruses (PRVs), have arisen from vertical inheritance of viral sequences integrated into host germline genomes. As viral genomic fossils, these sequences can thus serve as valuable paleogenomic data to study the long-term evolutionary dynamics of virus-virus interactions, but they have rarely been applied for this purpose. All extant PRVs have been considered autonomous species in their parasitic life cycle in host cells. Here, we provide evidence for multiple non-autonomous PRV species with structural defects in viral activity that have frequently infected ancient grass hosts and adapted through interplay between viruses. Our paleogenomic analyses using endogenous PRVs in grass genomes revealed that these non-autonomous PRV species have participated in interplay with autonomous PRVs in a possible commensal partnership, or, alternatively, with one another in a possible mutualistic partnership. These partnerships, which have been established by the sharing of noncoding regulatory sequences (NRSs) in intergenic regions between two partner viruses, have been further maintained and altered by the sequence homogenization of NRSs between partners. Strikingly, we found that frequent region-specific recombination, rather than mutation selection, is the main causative mechanism of NRS homogenization. Our results, obtained from ancient DNA records of viruses, suggest that adaptation of PRVs has occurred by concerted evolution of NRSs between different virus species in the same host. Our findings further imply that evaluation of within-host NRS interactions within and between populations of viral pathogens may be important.