Grafting is a common horticultural practice used to confer desirable traits between rootstock and scion, including disease resistance. To investigate graft‐conferred resistance against viral diseases a novel heterografting system was developed using
MSH1-induced heritable enhanced growth vigor through grafting is associated with the RdDM pathway in plants
Abstract Plants transmit signals long distances, as evidenced in grafting experiments that create distinct rootstock-scion junctions. Noncoding small RNA is a signaling molecule that is graft transmissible, participating in RNA-directed DNA methylation; but the meiotic transmissibility of graft-mediated epigenetic changes remains unclear. Here, we exploit the MSH1 system in Arabidopsis and tomato to introduce rootstock epigenetic variation to grafting experiments. Introducing mutations dcl2 , dcl3 and dcl4 to the msh1 rootstock disrupts siRNA production and reveals RdDM targets of methylation repatterning. Progeny from grafting experiments show enhanced growth vigor relative to controls. This heritable enhancement-through-grafting phenotype is RdDM-dependent, involving 1380 differentially methylated genes, many within auxin-related gene pathways. Growth vigor is associated with robust root growth of msh1 graft progeny, a phenotype associated with auxin transport based on inhibitor assays. Large-scale field experiments show msh1 grafting effects on tomato plant performance, heritable over five generations, demonstrating the agricultural potential of epigenetic variation.
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- Award ID(s):
- 1853519
- NSF-PAR ID:
- 10302572
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 11
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Nicotiana benthamiana scions grafted onto different tomato rootstocks.N. benthamiana is normally highly susceptible to tobacco mosaic virus (TMV) infection. However, specific tomato rootstock varieties were found to confer a range of resistance levels toN. benthamiana scions inoculated with TMV. Conferred resistance was associated with delays in virus accumulation and the reduction in virus spread. RNA sequencing analysis showed the enrichment of transcripts associated with disease resistance and plant stress inN. benthamiana scions grafted onto resistance‐inducing tomato rootstocks. Genome sequencing of resistance‐ and nonresistance‐conferring rootstocks was used to identify mobile tomato transcripts withinN. benthamiana scions. Within resistance‐inducedN. benthamiana scions, enriched mobile tomato transcripts were predominantly associated with defence, stress, and abscisic acid signalling when compared to similar scions grafted onto nonresistance‐inducing rootstock. Combining these findings suggests that graft‐induced resistance is modulated by rootstock scion transcriptional responses and rootstock‐specific mobile transcripts. -
The appropriate selection of rootstock-scion combinations to improve yield and fully realize grafting benefits requires an in-depth understanding of rootstock-scion synergy. Toward this end, we grafted two determinate-type scions [grape tomato (‘BHN 1022') and beefsteak tomato (‘Skyway')] onto four rootstocks with different characteristics to examine plant growth, yield performance, biomass production, and fruit mineral nutrient composition. The study was conducted during two growing seasons (spring and fall plantings in Florida) under organic production in high tunnels with the non-grafted scions as controls. Rootstocks had previously been designated as either “generative” (‘Estamino') or “vegetative” (‘DR0141TX') by some commercial suppliers or had not been characterized [‘RST-04-106-T' and ‘SHIELD RZ F1 (61-802)']. Also, ‘Estamino', ‘DR0141TX', and ‘RST-04-106-T' had been described as more vigorous than ‘SHIELD RZ F1 (61-802)'. In both planting seasons (with low levels of soilborne disease pressure), the “vegetative” and “generative” rootstocks increased marketable and total fruit yields for both scions except for the beefsteak tomato grafted with the “vegetative” rootstock in fall planting. Positive effects of ‘RST-04-106-T' on fruit yield varied with scions and planting seasons, and were most manifested when grafted with the beefsteak tomato scion in fall planting. ‘SHIELD RZ F1 (61-802)' led to similar yields as the non-grafted controls except for grafting with the grape tomato scion in fall planting. For vegetative and fruit biomass, both the “vegetative” and “generative” rootstocks had positive impacts except for the beefsteak tomato in fall planting. For fruit mineral composition, the “vegetative” and “generative” rootstocks, both highly vigorous, consistently elevated fruit P, K, Ca, Zn, and Fe contents on a dry weight basis, whereas the other rootstocks did not. Overall, although the more vigorous rootstocks enhanced tomato plant productivity and fruit minerals, the evidence presented here does not support the suggestion that the so-called “vegetative” and “generative” rootstocks have different impacts on tomato scion yield, biomass production, or fruit mineral contents. More studies with different production systems and environmental conditions as well as contrasting scion genotypes are needed to further categorize the impacts of rootstocks with different vigor and other characteristics on plant biomass production and their implications on fruit yield development.more » « less
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SUMMARY Sensory plastids are important in plant responses to environmental changes. Previous studies show that
MutS HOMOLOG 1 (MSH1 ) perturbation in sensory plastids induces heritable epigenetic phenotype adjustment. Previously, the PsbP homolog DOMAIN‐CONTAINING PROTEIN 3 (PPD3), a protein of unknown function, was postulated to be an interactor with MSH1. This study investigates the relationship of PPD3 with MSH1 and with plant environmental sensing. Theppd3 mutant displays a whole‐plant phenotype variably altered in growth rate, flowering time, reactive oxygen species (ROS) modulation and response to salt, with effects on meristem growth. Present in both chloroplasts and sensory plastids, PPD3 colocalized with MSH1 in root tips but not in leaf tissues. The suppression or overexpression of PPD3 affected the plant growth rate and stress tolerance, and led to a heritable, heterogenous ‘memory’ state with both dwarfed and vigorous growth phenotypes. Gene expression and DNA methylome data sets from PPD3‐OX and derived memory states showed enrichment in growth versus defense networks and meristem effects. Our results support a model of sensory plastid influence on nuclear epigenetic behavior andppd3 as a second trigger, functioning within meristem plastids to recalibrate growth plasticity. -
Previous studies of tomato rootstock effects on fruit quality have yielded mixed results, and few attempts have been made to systematically examine the association between rootstock characteristics and tomato fruit quality. In this study, grape tomato (‘BHN 1022’) and beefsteak tomato (‘Skyway’) were grafted onto four rootstocks [‘Estamino’ (vigorous and “generative”), ‘DR0141TX’ (vigorous and “vegetative”), ‘RST-04-106-T’ (uncharacterized), and ‘SHIELD RZ F1 (61–802)’ (mid-vigor, uncharacterized)] and compared to non-grafted scion controls for two growing seasons (Spring and Fall in Florida) in organically managed high tunnels. In both seasons and for both scions, the two vigorous rootstocks, regardless of their designation as “vegetative” (‘DR0141TX’) or “generative” (‘Estamino’), exhibited negative impacts on dry matter content, soluble solids content (SSC), SSC/titratable acidity (TA), lycopene, and ascorbic acid contents. Similar effects on fruit dry matter content and SSC were also observed with the ‘RST-04-106-T’ rootstock, although little to no change was seen with grafting onto ‘SHIELD RZ F1 (61–802)’. Further studies are needed to elucidate the impact of rootstock vigor on tomato volatile profiles and consumer sensory acceptability in order to better determine whether any of the documented effects are of practical importance. On the other hand, the evident effects of scion cultivar and planting season on fruit quality were observed in most of the measurements. The scion by rootstock interaction affected fruit length, firmness, pH, and total phenolic content, while the planting season by rootstock interaction impacted fruit firmness, pH, total antioxidant capacity, and ascorbic acid and lycopene contents. The multivariate separation pattern of planting season, scion, and rootstock treatments as revealed by the canonical discriminant analysis further indicated that the influence of scion cultivar and planting season on tomato fruit quality could be much more pronounced than the rootstock effects. The fruit color ( C * and H °), length and width, SSC, pH, total antioxidant capacity, ascorbic acid, and lycopene contents were the main attributes distinguishing different scion-planting season groups.more » « less
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Abstract Background Plants are naturally associated with root microbiota, which are microbial communities influential to host fitness. Thus, it is important to understand how plants control root microbiota. Epigenetic factors regulate the readouts of genetic information and consequently many essential biological processes. However, it has been elusive whether RNA-directed DNA methylation (RdDM) affects root microbiota assembly. Results By applying 16S rRNA gene sequencing, we investigated root microbiota of Arabidopsis mutants defective in the canonical RdDM pathway, including dcl234 that harbors triple mutation in the Dicer-like proteins DCL3, DCL2, and DCL4, which produce small RNAs for RdDM. Alpha diversity analysis showed reductions in microbe richness from the soil to roots, reflecting the selectivity of plants on root-associated bacteria. The dcl234 triple mutation significantly decreases the levels of Aeromonadaceae and Pseudomonadaceae , while it increases the abundance of many other bacteria families in the root microbiota. However, mutants of the other examined key players in the canonical RdDM pathway showed similar microbiota as Col-0, indicating that the DCL proteins affect root microbiota in an RdDM-independent manner. Subsequently gene analysis by shotgun sequencing of root microbiome indicated a selective pressure on microbial resistance to plant defense in the dcl234 mutant. Consistent with the altered plant-microbe interactions, dcl234 displayed altered characters, including the mRNA and sRNA transcriptomes that jointly highlighted altered cell wall organization and up-regulated defense, the decreased cellulose and callose deposition in root xylem, and the restructured profile of root exudates that supported the alterations in gene expression and cell wall modifications. Conclusion Our findings demonstrate an important role of the DCL proteins in influencing root microbiota through integrated regulation of plant defense, cell wall compositions, and root exudates. Our results also demonstrate that the canonical RdDM is dispensable for Arabidopsis root microbiota. These findings not only establish a connection between root microbiota and plant epigenetic factors but also highlight the complexity of plant regulation of root microbiota.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s41467-020-19140-x
