At least four dry, hot springs in a row have made an impact on recent cherry productions. This has generally led to good results in pre and post-harvest; however, there is a phytopatogen called Botrytis that we must never underestimate, since it can manifest and respond to small environmental changes, causing issues everywhere from the orchard to the final sale.
Botrytis, the superpathogen
Botrytis cinerea is probably the most relevant pathogen in Chilean fruit growing, a majority of the costs in phytosanitary management programs for table grapes, blueberries, strawberries and cherries are directed to control this fungus. Its versatility in terms of colonizing hosts is one of the features that lead us to categorize Botrytis as a SUPERPATHOGEN. Its first superpower that we must delve into is polyphagia.
Even though in Chile, as in other countries, we have been unable to observe sexual reproduction in this fungus, asexual reproduction is more than enough for it to reach an extremely high colonization rate due to its astonishing capacity to produce conidia (spores).
Photo 1. Sporulated Botrytis cinerea mycelium. In detail, conidiophores charged with conidia. Source: Diagnofruit/Res. Plant Dis. (2014) 20(4):275-282.
The pathogen’s capacity for adaptation, or “fitness”, is another feature that can be considered a superpower. Even though it has an optimal temperature range for growth, which is between 15 and 25ºC (between 18 and 20ºC in Chilean populations), it can also develop at temperatures as low as 0ºC, which allows for attacks on cherries in refrigerated storage. Obviously, improperly chilled fruit and improperly stowed or faulty containers are the ideal scenario for this fungus, which also always follows the same rule: the higher the temperature, the greater the rot development.
A secret weapon it possesses is its enzyme battery (essentially pectinase), which allows it to penetrate healthy epidermes, installing infection in fruits. Indiscriminate use of growth regulators, unbalanced fruits (high nitrogen and low calcium), bruises and other factors lay the groundwork for a more effective interaction between pathogen and fruit, allowing the fungus to more easily colonize it, even at refrigerated storage temperatures, as was previously stated.
As can be seen in the Fungicide Resistance Action Committee’s (FRAC) risk list, Botrytis cinerea has been assigned the highest risk grade in accordance with its pathogenic nature – a Level 3. It shares risk grades with other important well-known menaces like Penicillium or Venturia (Table 1); which, combined with the type of fungicide to be used depending on its inherent risk, can sometimes generate the greatest known combined risk of resistance – a 9 on the scale (Table 1). This means that this superpathogen, aside from the features we have already described, can very easily make changes in its own genome, making it a fungus that is capable of generating resistance to the fungicides we commonly use to control it.
This inherent capacity that Botrytis has of “changing” through the generation of specific mutations in its genome which in turn make it so the fungicide’s target protein modifies its own structure, leads to no activity from the fungicide or alternatively the overproduction of certain proteins in the fungus’s membrane that are capable of expelling the fungicide from the cell, limiting its action. These are strategies that the fungus uses in a very “intelligent” way to withstand and adapt in a hostile environment. But if the environment is too hostile – temperatures that are generally too low, nourishment scarcity or another limiting factor – this fungus has the capability to resist. So, what does it do? It builds what we call “sclerotia”, which are resistance structures that are formed by compacting the mycelium, where the fungus reduces its metabolic activity down to what we could consider a period of “hibernation”, waiting for better conditions before reactivating and continuing its life cycle.
Table 1. Diagram of combined resistance risk based on the fungicide’s inherent risk and the pathogen’s inherent risk. *Only the most important classes and groups of fungicides have been mentioned. **The risk of SDHI fungicides has been modified, from medium to medium-high. (Source: FRAC).
Photo 2. Botrytis cinerea sclerotium formed in the middle of an Agar-Potato-Dextrose harvest (PDA). Source: Diagnofruit.
As any self-respecting supervillain, it also has its own multiverse, in which Botrytis cinerea is the version we know the most, but there are also cryptic species (which we can only distinguish through genetic analyses) that somewhat frequently coexist in the same “dimension”. Even though we have no records in cherries, species like B. pseudocinerea and B. prunorum have been detected in table grapes and kiwis, respectively, living side by side with B. cinerea; though it’s important to point out that the latter is always dominant and therefore the one that control must be aimed at, at least in the immediate period – though climate change might modify this reality.
Botrytis presents two versions of disease in cherries, which would be, in phenological order:
i)Flower-infecting smut: most frequently takes place during warm, humid springs, the conidia colonize stamens and pistils and thus begins an infectious process that ends with the rot of the complete flower. The latest seasons in Chile have not provided the environmental conditions for the expression of this disease.
ii)Gray mold in fruits (pre- and post-harvest): once the fruit’s maturity increases, therefore generating more dry matter, more soluble solids and less acidity, it becomes more susceptible to Botrytis infections; thus the conidia that fall on the fruit’s epidermis are capable of degrading tissues and beginning to feed on the carbohydrates that abound in the pulp during this stage, allowing for a profuse generation of conidia and grey mycelium at room temperature, and white mycelium if the process occurs during refrigerated storage. Rain during pre-harvest leads to the ideal conditions for the development of this fungus, where each tear is an ideal entry point for Botrytis and other secondary fungi. To prevent this, it is always better to apply before the climate event takes place, at least 24 hours before the rain. Even though the last two seasons have had little Botrytis inoculum in fields (Graph 1), we must always be vigilant about changes in this state of things, continuously monitoring and acting in a preventive manner.
Graph 1. Amount of average inoculum of B. cinerea in fruits during the past 4 seasons, calculated at harvest through qPCR considering 3 orchards in the Maule Region.
What has been described gives us signs of the critical moments at which we must perform applications to control for the pathogen:
i)Blooming, generally, two applications are recommended to avoid the feared smut; at initial bloom and full bloom are the moments that best prevent the disease’s development. Synthesis fungicides, vegetable extracts and/or biocontrollers can be used, alternating between types. In complex situations – orchards with histories, humid springs – two applications of botricides (carboxamides, hydro-oxyanilides or phenylpyrrole) must be programmed as a base and products of biological origin must be considered as support.
ii)Pre-harvest: the critical stage begins a few days after the straw-colored hue sets in and until harvest. Depending on the variety, whether it’s early or late, the window for applications is different. Having this in mind, a base program considers at least a couple of applications and up to four in varieties of extended development. Again, the base must be constructed with specific botricides and successive applications of extracts or biocontrollers. Even though Botrytis populations in cherry tress don’t generally offer resistance to fungicides, it is important, as a general anti-resistance measure, to try not to repeat fungicide applications of the same chemical groups more than 2 times in each season.
iii)Post-harvest: final moment for control. Due to the possibility of fruit immersion, applications in this stage are very effective. Fludioxonil is the standard fungicide for the control of this pathogen at post-harvest and the amount of residue it may leave on the fruit must be constantly monitored. Since the calibration process takes place in the water, it is easy for the Botrytis inoculum (as well as other fungi) to remain, contaminating the system. Therefore, to avoid contagion, some method of sanitation must also be performed. One of the most efficient routes is chlorine.
So, today we learned a bit more about Botrytis, this superpathogen that we now know not to underestimate, even when environmental conditions don’t appear to be the most optimal for this fungus. In this sense, we must be cautious and proactive, not allowing it to sneak in through some small fissure in the system. We should at least ensure compliance of minimal actions like observing spring conditions and environmental indicators that might predispose our crops to the development of this fungi and, ideally, have data on inoculum quantity present in our orchard; performing proper and timely cultural management that may allow for a successful control checklist that should at least consider the performance of a base fungicide program both in blooming and in pre-harvest. Don’t just leave the hard work in the hands of extracts and biocontrollers – even though it might seem like a “benign” season. And finally, don’t forget to take anti-resistance measures and monitor crops using the field’s history, thus avoiding the selection of Botrytis-prone populations, while maintaining balance so as to not generate resistance to fungicides in our orchards.