SUMMARY

• Two broccoli plantings immediately prior to growing the verticillium-susceptible crop is recommended for best protection
• Fresh broccoli residue has greater reduction in V. wilt than dry residue
• Field tarping following fresh residue incorporation did not increase (or decrease) efficacy
• Suppression of V. dahliae is specific to broccoli and not provided by other Brassicaceae crops.
• V. dahliae isolates from 15 host crops, including tomato, eggplant, bell pepper, lettuce, potato, watermelon and strawberry, were effectively suppressed by 5 broccoli cultivars
• The most significant reduction in V. dahliae occurs 15 days post-incorporation, and continues to decline over the season.
• More mature broccoli plants have higher levels of volatile antifungal substances
• The mechanisms of action are hypothesized to include: volatile antifungal compounds, changes in the soil microbial communities and serving as a ‘dead-end host'.
• Broccoli has been shown to reduce pathogens causing Verticillium wilt and lettuce drop, but not other soilborne pathogens such as Fusarium spp..

BACKGROUND

In 1999, several UC researchers published foundational research in a paper titled, “Evaluation of broccoli residue incorporation into field soil for Verticillium wilt control in cauliflower.” Since this publication more than 20 years ago, many studies have further investigated this concept and many coastal growers, especially organic producers, have adopted broccoli rotations as a strategy for Verticillium wilt control. Today, typical implementation of this strategy is two broccoli plantings back to back prior to the crop for which Verticillium wilt suppression is desired. While California coastal vegetable production has been the framework for much of this work, the adaptability of this practice to the Sacramento Valley is very promising for management of Verticillium wilt in warm and cool season crops[1].

Verticillium wilt is caused by the soilborne fungal pathogen Verticillium dahliae. Microsclerotia, the fungal inoculum that causes infection, dwell in the soil until root exudates stimulate germination and direct the fungal hyphae towards the root. In susceptible plants, infection occurs when hyphae enter the roots right behind the root tip, and continue growth into the water-conducting vascular tissue, the xylem. Once in the xylem, hyphal growth and sporulation can move the fungus into the upper plant tissue. Plant death triggers the fungus to a reproductive stage, prompting microsclerotia formation. When infected crop residue is incorporated into the soil, microsclerotia in the crop residue are incorporated, too. Management is particularly challenging because the pathogen host range is over 300 crops and the inoculum survive upwards of 13 years (1). To establish control of the pathogen, the key is to reduce inoculum—the number of microsclerotia, below levels damaging to susceptible crops.

Microsclerotia in crop residue

Image:Thousands of microsclerotia, small, black propagules of V. dahliae, formed on susceptible crop residue and remained intact post residue incorporation. Photo credit: M. Lloyd

BROCCOLI SUPPRESSES VERTICILLIUM WILT AND DECREASES PATHOGEN PROPAGULES

Broccoli is one of the few non-host vegetables and member of the Brassicaceae family. Bok choy, broccoli raab, Brussels sprouts, cabbage, cauliflower, Chinese cabbage, and rapini are susceptible to V. dahliae, as are black mustard, Indian mustard, oilseed rape, and turnip. In broccoli, no infection to minor infection from V. dahliae has been observed. In the case of minor infections, the pathogen does not progress beyond the roots and microsclerotia formation in the roots is repressed. Apart from the importance of selecting a non-host as a rotation crop, the glucosinolate profile of broccoli, the secondary compounds responsible for the toxic effect, differs from other brassicaceous crops

Following broccoli residue incorporation, research out of Japan demonstrated Verticillium wilt incidence of eggplant decreased by 53 % compared to eggplant without broccoli rotation (2, 3). In California Cauliflower production, disease incidence and severity were both reduced approximately 50% following broccoli residue treatments.

Broccoli did not just decrease disease incidence, but decreased the amount of pathogen inoculum (2), showing promise for longer term management. In a California study, overall reduction in the number of propagules in V. dahliae-infested plots after two broccoli crops was approximately 94%, in contrast to the five-fold increase in the number of propagules after two cauliflower crops (4). These findings corroborate earlier studies showing reductions in the numbers of soilborne microsclerotia of V. dahliae and incidence of wilt on cauliflower that were comparable to reductions caused by chloropicrin and metham sodium treatments (5). Importantly, following broccoli rotations, microsclerotia continue to decline through-out the following cropping season and remain low during the following season. In contrast, propagules in soil fumigated with chloropicrin and metham sodium declined initially but later returned to pre-treatment levels by the end of the cropping season.

MECHANISM OF SUPPRESSION

Shetty et al. (2000) reported that the effects of broccoli in reducing microsclerotia and suppressing disease may be associated with the following mechanisms: (1) production of volatile antifungal substances such as allyl-isothiocyanate (ITC) by broccoli residue, (2) increase in antagonistic microorganisms, and (3) degradation of microsclerotia melanin by ligninase/melaninase produced by soil microorganisms in the presence of broccoli lignin. ITCs are chemically similar to methylisothiocyanate, the active agent from the chemical fumigant metam sodium. Likely associated with the ability to generate these conditions, fresh broccoli residue was shown to be more suppressive than dry residue. During tissue decomposition, the glucosinolates in crucifer crops, the characteristic sulfur-containing constituents of the members of Brassicaceae responsible for their inherent pungent odor, break down to produce sulfides, isothiocyanates, thiocyanates, and nitriles that have either fungistatic or fungicidal properties (6). In addition to release of toxic compounds and microbial activity provided by broccoli residue, the plant may be serving as a ‘decoy', ‘trap crop' or ‘dead end host', further driving population numbers down (2). As described earlier, some V. dahliae infection is observed in broccoli roots, but it does not result in microsclerotia formation. By stimulating inoculum germination and preventing fungal reproduction, the number of viable microsclerotia decrease in the soil.

GROWER IMPLEMENTATION OF RESEARCH FINDINGS

To facilitate greater adaptation of rotations with broccoli in other crops susceptible to V. dahliae, Bhat and Subbarao asked the question whether isolates of V. dahliae originating from different susceptible hosts could cause wilt on broccoli. They evaluated 15 different host isolates against multiple broccoli varieties. This included tomato, eggplant, bell pepper, lettuce, potato, watermelon and strawberry, and found that only isolates from cabbage and cauliflower were weakly pathogenic. Broccoli cultivars Baccus, Greenbelt, Parasol, Patriot, and Symphony showed resistance to Verticillium infection (3). This provides some evidence for the usefulness of this method in other cropping systems.

Implementation of broccoli rotations for Verticillium wilt management is optimized when two successive broccoli crops are grown immediately prior to desired Verticillium wilt reduction. Higher amounts of glucosinolates, specifically glucobrassicin, are found in older plants. Research has reported a complete absence of glucobrassicin in broccoli seedlings, 50% of the total in immature heads (5-10 cm diameter) and the highest levels at fully developed Packman broccoli heads (15-20 cm diameter) (7). These results suggest that glucobrassicin synthesis is active during later stages of broccoli development. Plants should be mowed and finely chopped in order to disrupt the plant cells as much as possible. The greatest reductions in microsclerotia occur at soil temperatures above 68°F, and most of this reduction occurs within 15-30 days of incorporation (8). Variation in efficacy of this method is attributed to multiple factors: fluctuation in climate and cultivation conditions, physical and chemical properties of the soil, soil microbial properties, the type of broccoli cultivar used, differences in pathogen density, and variance in the susceptibility of the following crop host. The types and amounts of glucosinolates vary with the crucifer species and determine the level of plant pathogen growth reduction.

This practice could also have other potential benefits and drawbacks. Growers in California have observed for many years that where broccoli residues from processing plants are dumped onto a field, weed populations are reduced the following year (5). Thus, rotations with broccoli may have multiple pest management benefits. However, in recent years in the Sacramento Valley, crop damage from bagrada bug has been significant. Although these outbreaks have largely occurred in fall, outbreaks have occurred in the spring in this region. Members of the Brassicaceae family are the host plants for bagrada and under favorable environmental conditions would support this pest population.

This management strategy is specific to Verticillium dahliae and is not transferrable to other soilborne pathogens such as Fusarium spp.. Because these two pathogens are common in the Sacramento Valley and above ground symptoms are similar, diagnosis is important. Contact me at any time for disease diagnostic support. All visits and sample analyses are provided free of charge.

SUGGESTED READING

Koike S, Subbarao K. 2000. Broccoli residues can control Verticillium wilt of cauliflower. Calif Agr 54(3):30-33. https://doi.org/10.3733/ca.v054n03p30.

http://calag.ucanr.edu/archive/?type=pdf&article=ca.v054n03p30

REFERENCES

1 Schnathorst, W. C. 1981. Life cycle and epidemiology of Verticillium. Pages 81-111 in: Fungal Wilt Diseases of Plants. M. E. Mace, A. A. Bell, and C. H. Beckman, eds. Aca-demic Press, New York.

2 Ikeda, K., Banno, S., Furusawa, A. et al. Crop rotation with broccoli suppresses Verticillium wilt of eggplant. J Gen Plant Pathol 81, 77–82 (2015).

3 Bhat, R. G., and Subbarao, K. V. 2001. Reaction of broccoli to isolates of Verticillium dahliae from various hosts. Plant Dis. 85:141-146.

4 Xiao, C. L., Subbarao, K. V., Schulbach, K.F., and Koike, S. T. 1998. Effects of crop rotation and irrigation on Verticillium dahliae microsclerotia in soil and wilt in cauliflower. Phytopathology 88:1046-1055.

5 Subbarao, K. V., Hubbard, J. C., and Koike,S. T. 1999. Evaluation of broccoli residue incorporation into field soil for Verticillium wilt control in cauliflower. Plant Dis.83:124-129.

6 Gamliel, A., and Stapleton, J. J. 1993. Characterization of antifungal volatile compounds evolved from solarized soil amended with cabbage residues. Phytopathology 83:899-905.

7 Kushad, M.M., B.P. Klein, M.A. Wallig, E.H. Jeffery, A.F. Brown, and A.C. Kurilich. 1999. Variation of glucosinolates in vegetable crops of Brassicaoleracea. J. Agr. Food Chem. 47:1541–1548.

8 Subbarao, K. V., and Hubbard, J. C. 1996.Interactive effects of broccoli residue and temperature on Verticillium dahliae microsclerotia in soil and on wilt in cauliflower. Phytopathology 86:1303-1310.

[1] Research has also demonstrated suppression of lettuce drop caused by Sclerotinia minor from broccoli residue. Hao J, Subbarao KV, Koike ST (2003) Effects of broccoli rotation on lettuce drop caused by Sclerotinia minor and on the population density of sclerotia in soil. Plant Dis 87:159–166.

Nitrogen is one of the essential macronutrients required for a healthy, productive crop. With summer in full swing, the nitrogen demand for many crops is high.  Use these graphs to understand the timing of nitrogen demand in the crops you are growing. Soil tests and tissue tests are great ways to know the current nitrogen status of your soil or crop to determine whether you have sufficient nitrogen to meet the demand. Click to learn more about soil and tissue sampling.

Visit Dr. Daniel Geisselers Lab and CDFA Fertilizer Research and Education Program for more information. 

Here's a GENERAL N UPTAKE CURVE FOR ANNUALS . Click here for more information.

N Uptake Curve for MELONS. Click here for more information.

N Uptake Curve for Fresh Market Tomatoes. Click here for more information

N Uptake Curve for PLUMS AND PRUNES. Click here for more information

N Uptake Curve for STRAWBERRIES. Click here for more information. 

N Uptake Curve for PEACHES AND NECTARINES. Click here for more information. 

Tomato spotted wilt virus (TSWV), transmitted by western flower thrips (Frankliniella occidentalis), is widespread in Yolo/Solano/Sacramento county and can cause severe damage to fresh market tomatoes and peppers.  Using a piercing-sucking mouthpart, thrips damage appears as small white/silver/grey patches (see photo). To confirm the presence of thrips, lightly shake a plant onto your hand or a dark surface and use a hand lens to look for the insect, or take a hand lens to the leaf damage and check for thrips. Young plants infected with TSWV are stunted with leaf bronzing (see photo), while mature plants have green and red fruit that are bumpy and deformed and typically show diagnostic ringspots (often concentric in green fruits).  TSWV diagnosis can be made onsite using an ImmunoStrip, available from your local farm advisor.

Thrips damage

TSWV in a young tomato plant

In the spring, the first or second generation of thrips are mostly free of the virus. After breeding on plant reservoirs infected with the virus, third generation virus-carrying winged adults can start spreading TSWV into crops, especially pepper and tomato. Virus reservoirs include weedy species and some cultivated ones including fava beans, lettuce and radicchio. New findings suggest that another early season reservoir is infected pupae overwintering in soil.  Once the crop has some level of viral infection, the weeds become much less important, simply because the sheer number and density of infected crop plants (peppers and tomatoes) generally outnumbers the presence of weeds. For this reason, diligently rogueing young, symptomatic plants can significantly benefit your stand and is an important part of increasing the efficacy of a spray program. In the case of processing tomatoes, plants are sensitive to attack pre-flowering.  Once fruit is set, new infections tend to only cause "strikes" that kill or damage only one branch, but large plants are rarely killed and the fruit is still usable for paste. This has not been verified for fresh market tomatoes, but can be considered when making your own observations over the season. 

What that means for virus control is that there's a window of a couple of months when the crop is at risk - corresponding to the third, fourth and maybe fifth generations of thrips. The Gilbertson and McRoberts lab in the UC Davis Department of Plant Pathology have developed a degree-day model to track and predict thrips generations. Here, you can see the status for Yolo County, which says on June 3 we are at Generation 2, peak adult. Generation 3, peak adult is expected to be June 28. By managing thrips populations during this Generation 2 window, plants are allowed the chance to grow past the danger period and, importantly, the number of virus-carrying adult thrips is reduced early in the season, thereby slowing overall spread. Fresh market production may differ in that infection is likely a problem at any time because virus symptoms on fruit will make them unmarketable.  However, the differences between fresh market and processing tomatoes have not been examined. 

Genetic resistance is available.  Varieties with the Sw5 gene are resistant to infection and do not show symptoms (in pepper there is another gene, Tsw, that confers resistance to TSWV). Originally isolated from wild tomato species from Peru, traditional breeding is being used to develop resistant cultivars that are effective against new resistance-breaking (RB) strains of TSWV. Resistance-breaking (RB) TSWV strains are present in California and other parts of the world, but are currently not very prevalent in Northern California.

Organic pesticide control of thrips is challenging, but can potentially play a role  in reducing the impact and/or timing of an infection. Organically approved products for thrips control include  spinosad or pyrethrum-based products, in addition to some botanicals. It's often important to combine a product with an adjuvant such as Oroboost, Vista Sil or others to increase leaf coverage and residual activity. Regular applications will be required for continued thrips control. Alternatively, protection from thrips can also be achieved by protecting plants with insect nets early in the season.   

Do you control for thrips? If so, how? Are you growing fresh market varieties with TSWV-resistance? I'd love to hear your story.

Thanks to the UCD Department of Plant Pathology—Bob Gilbertson and Neil McRoberts, for their contributions to this article.