scholarly journals Comparative Analysis of the Apple Root Transcriptome as Affected by Rootstock Genotype and Brassicaceae Seed Meal Soil Amendment: Implications for Plant Health

2021 ◽  
Vol 9 (4) ◽  
pp. 763
Author(s):  
Likun Wang ◽  
Tracey S. Somera ◽  
Heidi Hargarten ◽  
Loren Honaas ◽  
Mark Mazzola

Brassicaceae seed meal (SM) soil amendment has been utilized as an effective strategy to control the biological complex of organisms, which includes oomycetes, fungi, and parasitic nematodes, that incites the phenomenon termed apple replant disease. Soil-borne disease control attained in response to Brassicaceae SM amendment is reliant on multiple chemical and biological attributes, including specific SM-generated modifications to the soil/rhizosphere microbiome. In this study, we conducted a comparative analyses of apple root gene expression as influenced by rootstock genotype combined with a seed meal (SM) soil amendment. Apple replant disease (ARD) susceptible (M.26) and tolerant (G.210) rootstocks cultivated in SM-amended soil exhibited differential gene expression relative to corresponding non-treated control (NTC) orchard soil. The temporal dynamics of gene expression indicated that the SM-amended soil system altered the trajectory of the root transcriptome in a genotype-specific manner. In both genotypes, the expression of genes related to plant defense and hormone signaling were altered in SM-amended soil, suggesting SM-responsive phytohormone regulation. Altered gene expression was temporally associated with changes in rhizosphere microbiome density and composition in the SM-treated soil. Gene expression analysis across the two rootstocks cultivated in the pathogen-infested NTC soil showed genotype-specific responses indicative of different defensive strategies. These results are consistent with previously described resistance mechanisms of ARD “tolerant” rootstock cultivars and also add to our understanding of the multiple mechanisms by which SM soil amendment and the resulting rhizosphere microbiome affect apple rootstock physiology. Future studies which assess transcriptomic and metagenomic data in parallel will be important for illuminating important connections between specific rhizosphere microbiota, gene-regulation, and plant health.

2019 ◽  
Vol 109 (4) ◽  
pp. 607-614 ◽  
Author(s):  
Likun Wang ◽  
Mark Mazzola

Preplant soil application of a Brassica juncea–Sinapis alba seed meal formulation (SM) at a rate of 6.6 t ha−1 alters composition of the orchard soil microbiome in a manner that yields sustainable long-term suppression of soilborne pathogens in apple production systems. However, the cost of SM amendment has hindered the adoption of this tactic to manage apple replant disease in commercial orchards. Greenhouse trials were conducted to assess the effect of reduced SM application rates in concert with apple rootstock genotype on structure of the rhizosphere microbiome and associated disease control outcomes. At all application rates assessed, SM treatment increased tree growth and reduced disease development relative to the control. In general, total tree biomass and leader shoot length were similar in soils treated with SM at 4.4 or 6.6 t ha−1 regardless of rootstock genotype. Equivalent increase in tree biomass when cultivated in soil treated at the lowest and highest SM amendment rate was attained when used in conjunction with G.41 or G.210 apple rootstocks. Suppression of Pythium spp. or Pratylenchus penetrans root densities was similar at all SM application rates. When cultivated in nontreated replant orchard soil, Geneva rootstocks (G.41 and G.210) exhibited lower levels of Pythium spp. and P. penetrans root colonization relative to Malling rootstocks (M.9 and MM.106). For a given rootstock, structure of the rhizosphere microbiome was similar in soils treated with SM at 4.4 and 6.6 t ha−1. G.41 and G.210 rootstocks but not M.9 or MM.106 cultivated in soil treated with SM at 2.2 t ha−1 possessed a rhizosphere bacterial community structure that differed significantly from the control. Findings indicate that effective control of apple replant disease may be attained at lower SM amendment rates than employed previously, with lower effective rates possible when integrated with tolerant rootstock genotypes such as G.41 or G.210.


2015 ◽  
Vol 105 (4) ◽  
pp. 460-469 ◽  
Author(s):  
Mark Mazzola ◽  
Shashika S. Hewavitharana ◽  
Sarah L. Strauss

Brassicaceae seed meal (SM) formulations were compared with preplant 1,3-dichloropropene/chloropicrin (Telone-C17) soil fumigation for the ability to control apple replant disease and to suppress pathogen or parasite reinfestation of organic orchard soils at two sites in Washington State. Preplant soil fumigation and an SM formulation consisting of either Brassica juncea–Sinapis alba or B. juncea–B. napus each provided similar levels of disease control during the initial growing season. Although tree growth was similar in fumigated and SM-amended soil during the initial growing season, tree performance in terms of growth and yield was commonly superior in B. juncea–S. alba SM-amended soil relative to that in fumigated soil at the end of four growing seasons. SM-amended soils were resistant to reinfestation by Pratylenchus penetrans and Pythium spp. relative to fumigated soils and corresponded with enhanced tree performance. Phytotoxic symptoms were observed in response to SM amendment at one of two orchard sites, were dependent upon season of application, and occurred in an SM formulation-specific manner. After 2 years, the rhizosphere microbiome in fumigated soils had reverted to one that was indistinguishable from the no-treatment control. In contrast, rhizosphere soils from the SM treatment possessed unique bacterial and fungal profiles, including specific microbial elements previously associated with suppression of plant-pathogenic fungi, oomycetes, and nematodes. Overall diversity of the microbiome was reduced in the SM treatment rhizosphere, suggesting that enhanced “biodiversity” was not instrumental in achieving system resistance or pathogen suppression.


Author(s):  
Alicia Balbín-Suárez ◽  
Samuel Jacquiod ◽  
Annmarie-Deetja Rohr ◽  
Benye Liu ◽  
Henryk Flachowsky ◽  
...  

Abstract A soil column split-root experiment was designed to investigate the ability of apple replant disease (ARD) causing agents to spread in soil. ‘M26’ apple rootstocks grew into a top layer of Control soil, followed by a barrier-free split-soil layer (Control soil/ARD soil). We observed a severely reduced root growth, concomitant with enhanced gene expression of phytoalexin biosynthetic genes and phytoalexin content in roots from ARD soil, indicating a pronounced local plant defense response. Amplicon sequencing (bacteria, archaea, fungi) revealed local shifts in diversity and composition of microorganisms in the rhizoplane of roots from ARD soil. An enrichment of OTUs affiliated to potential ARD fungal pathogens (Ilyonectria and Nectria sp.) and bacteria frequently associated with ARD (Streptomyces, Variovorax) was noted. In conclusion, our integrated study supports the idea of ARD being local and not spreading into surrounding soil, as only the roots in ARD soil were affected in terms of growth, phytoalexin biosynthetic gene expression, phytoalexin production, and altered microbiome structure. This study further reinforces the microbiological nature of ARD, being likely triggered by a disturbed soil microbiome enriched with low mobility ARD-causing agents that induce a strong plant defense and rhizoplane microbiome dysbiosis, concurring with root damage.


2019 ◽  
Vol 109 (8) ◽  
pp. 1378-1391 ◽  
Author(s):  
Likun Wang ◽  
Mark Mazzola

An orchard field trial was conducted to assess the utility of reduced rate Brassicaceae seed meal (SM) amendment in concert with specific rootstock genotypes for effective control of apple replant disease. Three amendment rates of a 1:1 formulation of Brassica juncea-Sinapis alba SM were compared with preplant 1,3-dichloropropene/chloropicrin soil fumigation for disease control efficacy. When applied at the highest rate (6.6 t ha−1) in the spring of planting, SM caused significant phytotoxicity and tree mortality, which was higher for Gala/M.26 than for Gala/G.41 but was not observed at SM application rates of 2.2 or 4.4 t ha−1. SM treatment resulted in growth and yield increases of Gala/M.26 and Gala/G.41 trees in a manner similar to the fumigation treatment and significantly greater than the no treatment control. Tree growth in soils treated with SM at 4.4 t ha−1 was similar or superior to that obtained with SM at 6.6 t ha−1 and superior to that attained at an SM application rate of 2.2 t ha−1. Soil fumigation and all SM treatments reduced Pratylenchus penetrans root infestation relative to the control treatment at the end of the initial growing season. Lesion nematode root densities in the fumigation treatment, but not SM treatments, rapidly recovered and were indistinguishable from the control at the end of the second growing season. Soil fumigation and all SM treatments significantly suppressed Pythium spp. root infection relative to the control. Trees grafted to rootstock G.41 possessed lower P. penetrans root densities relative to trees grafted to rootstock M.26. One year after planting, composition of microbial communities from SM-amended soils was distinct from those detected in control and fumigated soils, and the differences were amplified with increasing SM application rate. Specific fungal and bacterial phyla associated with suppression of plant pathogens were more abundant in SM-treated soil relative to the control, and they were similar in abundance in 4.4- and 6.6-t ha−1 SM treatments. Findings from this study demonstrated that use of the appropriate apple rootstock genotype will allow for effective replant disease control at SM application rates significantly less than that utilized previously (6.6 t ha−1).


2001 ◽  
Vol 91 (7) ◽  
pp. 673-679 ◽  
Author(s):  
Mark Mazzola ◽  
David M. Granatstein ◽  
Donald C. Elfving ◽  
Kent Mullinix

The impact of Brassica napus seed meal on the microbial complex that incites apple replant disease was evaluated in greenhouse trials. Regardless of glucosinolate content, seed meal amendment at a rate of 0.1% (vol/vol) significantly enhanced growth of apple and suppressed apple root infection by Rhizoctonia spp. and Pratylenchus penetrans. High glucosinolate B. napus cv. Dwarf Essex seed meal amendments did not consistently suppress soil populations of Pythium spp. or apple root infection by this pathogen. Application of a low glucosinolate containing B. napus seed meal at a rate of 1.0% (vol/vol) resulted in a significant increase in recovery of Pythium spp. from apple roots, and a corresponding reduction in apple seedling root biomass. When applied at lower rates, B. napus seed meal amendments enhanced populations of fluorescent Pseudomonas spp., but these bacteria were not recovered from soils amended with seed meal at a rate of 2% (vol/vol). Seed meal amendments resulted in increased soil populations of total bacteria and actinomycetes. B. napus cv. Dwarf Essex seed meal amendments were phytotoxic to apple when applied at a rate of 2% (vol/vol), and phytotoxicity was not diminished when planting was delayed for as long as 12 weeks after application. These findings suggest that B. napus seed meal amendments can be a useful tool in the management of apple replant disease and, in the case of Rhizoctonia spp., that disease control operates through mechanisms other than production of glucosinolate hydrolysis products.


HortScience ◽  
1998 ◽  
Vol 33 (3) ◽  
pp. 531d-531
Author(s):  
Dorcas Isutsa ◽  
Ian Merwin ◽  
Bill Brodie

Apple replant disease (ARD) causes serious problems in most fruit-growing regions worldwide. It is associated with nematodes, fungi, bacteria, and other deleterious factors. Its symptoms range from severe stunting to death of replants in old orchards. We evaluated effects of antibacterial (cecropin-, attacin- and hen egg white lysozyme-encoding) and antifungal (chitinase-encoding) transgenics, obtained from the apple-rootstock breeding program at Geneva, N.Y., on ARD. Transgenics were tested in a composite soil collected from New York orchards with known replant problems. The ARD-infested field soil (FS) had ≈675 Pratylenchus penetrans (root-lesion nematodes, RLN) and ≈75 Xiphinema americanum (dagger nematodes) per liter pot; soil for controls was steam-pasteurized. Height, biomass, nematode vermiforms and eggs were recorded after ≈60 days under optimal growing conditions in the greenhouse. There was significant variation in growth and Pratylenchus counts among transgenics (P < 0.00), most of which were susceptible to ARD. However, endoparasitic RLN accounted for <50% of the variation in biomass, suggesting that other factors were important in affecting plants. Conversely, RLN significantly increased root necrosis (P < 0.00; R2 = 80%). Eggs were observed in diseased chitinase-encoding lines, probably because of low-gene expression. There was no significant difference in eggs among the lines (P ≤ 0.3). Apparently, good growth was inconsistent and due to confounding factors such as mild ARD. These results suggest that single-gene therapy and low-gene expression may not protect apple against ARD complex, instead gene-pyramiding and high-gene expression should be tested.


Plant Disease ◽  
2005 ◽  
Vol 89 (11) ◽  
pp. 1207-1213 ◽  
Author(s):  
Mark Mazzola ◽  
Kent Mullinix

Alternative management strategies to the use of preplant soil fumigation for the control of apple replant disease (ARD), including cover crops and strategies incorporating Brassica napus seed meal (rape seed meal [RSM]) amendment as the central component, were evaluated in the orchard. A 1-year wheat cover crop consisting of three short-term cropping periods with plant material removed at the end of each growth period and a 3-year B. napus green manure significantly enhanced vegetative growth and yield of Gala/M26. However, in each instance, the resulting disease control and growth response were inferior to that achieved through preplant methyl bromide soil fumigation. A 3-year bare fallow and 1- or 2-year B. napus green manure neither suppressed disease development nor enhanced tree growth. Preplant RSM amendment in conjunction with a postplant mefenoxam soil drench provided effective suppression of ARD, and the resulting tree growth and yield were comparable with that attained in response to 1,3- dichloropropene-chloropicrin fumigation in one orchard. At a second orchard, the growth response attained with the alternative treatment was inferior to preplant soil fumigation, which was associated with an apparent re-infestation of RSM-treated soils and tree roots by Pratylenchus spp. Application of RSM after wheat cropping or in conjunction with soil solarization provided an intermediate level of disease control and a corresponding reduction in growth and yield of apple relative to preplant fumigation at both sites.


2019 ◽  
Vol 3 (4) ◽  
pp. 273-285 ◽  
Author(s):  
Greg Deakin ◽  
Felicidad Fernández-Fernández ◽  
Julie Bennett ◽  
Tom Passey ◽  
Nicola Harrison ◽  
...  

Continuous plantation of apple trees (Malus pumila) at the same sites where the same or a closely related species were grown previously leads to poor establishment, reduced growth vigor, and subsequent crop losses; this phenomenon is termed apple replant disease (ARD). Management of ARD is a continual challenge due to (i) restrictions on the use of broad-spectrum soil fumigants, (ii) putative causal agents of ARD can be site-specific, and (iii) more than one causal agent can be present at a site. We conducted an experimental study at two orchard sites to investigate the succession effect of rootstock genotypes on apple tree establishment with three specific objectives: (i) whether ARD in newly planted apple trees is more severe if the same rootstock as the previous one is replanted, (ii) whether trees develop better in the aisle than in original tree stations, and (iii) the extent of association of rootstock genotypes with rhizosphere microbiome in relation to ARD. Tree growth and rhizosphere microbiome were assessed within 30 months of replanting. In one orchard, replanting trees with a rootstock genotype different from the previous one can be effective in reducing ARD development, susceptibility to ARD is likely to be genetically controlled, and replanting trees in the previous grass aisle can reduce ARD development. However, the opposite results were obtained in the other orchard, possibly due to the lack of weed management in the grass aisle affecting tree establishment in the grass aisle. Rhizosphere microbiota associated with specific rootstock genotypes reached a stable state within 7 months of replanting. An arbuscular mycorrhizal fungi operational taxonomic unit (OTU) had reduced abundance with ARD trees; however many other OTUs associated with ARD cannot be identified to low taxonomic ranks and hence their roles cannot be easily interpreted. In conclusion, replanting trees with rootstocks that are genetically differently from the previous one can reduce ARD development. However, in adopting this strategy, the extent of genetic relationships among rootstock genotypes needs to be considered.


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