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Flowers grow less yellow without sulphur, and that could affect the pollinators that need to see them

Both Van Gogh and Nature like to use sulphur-derived pigments for flowers, but what happens when there's not enough sulphur?

Plants use a variety of pigments to create the colours of their petals. These pigments are complex chemicals. If the plant doesn’t have access to the right nutrients, then its flowers will suffer. But which nutrients are the right nutrients? Ties Ausma and colleagues investigated the effects of sulphur, nitrogen and phosphorous limitation on various floral traits.

Sulphur is an often overlooked nutrient. Often you’ll read about N for nitrogen, P for phosphorus and sometimes K for Potassium, but not so much for S. In an email to Botany One, co-author Casper van der Kooi said, “Sulphur indeed is an often-overlooked nutrient, particularly when compared to the amount of research done on P and N. A lot agricultural land also suffers from S deficiency, but its occurrence and causes are largely unknown, so also a lot of farmers don’t know of it.”

First author Ties Ausma added that he had recently talked to farmers who have such aberrantly shaped flowers in their rapeseed crops, but they didn’t know it could be caused by sulphur deficiency. “Further, farmers increasingly use S-free fertilisers, instead of fresh manure that was more common back in the days, which, together with an increased crop density in agricultural fields, only exacerbates deficiency.”

A team based in Groningen, Graz and Cologne set up experiments to see how nutrient deficiencies, including sulphur, affected floral development and pollen traits. Two of the plants, Brassica rapa (the species that produces turnip and bok choy, among other things) and Physalis philadelphica (Tomatillo) have yellow flowers.

“Generally, yellow colors are generated by carotenoids, white flowers by flavonols, and blue, purple, and red colors by anthocyanin pigments,” van der Kooi writes in another recent paper. So it would be helpful to examine some plants with different coloured flowers. The team also included three Petunia species in their trials, Petunia nyctaginiflora, P. exserta and P. integrifolia. These plants provided white, purple and red flowers. This way, if a nutrient deficiency only inhibited the production of one set of pigments, then it should be clear.

The method for the experiment is interesting. After forming the first non-cotyledon leaves, the team transferred the seedlings to another container with a nutrient solution. All the seedlings spent a week in this solution. Then, the authors write in their paper, “After the formation of the first flower buds, which was after 7 days, plants were transferred to a fresh 25 % Hoagland nutrient solution at 0.5 mM (+S, sulphur-sufficient) or 0 mM sulphate (-S, sulphur-deprived).” So the sulphur stress occurred at a late stage, and it’s not a large difference in sulphur concentration. There is a good reason for this, Ausma and van der Kooi write in their email.

“What matters is that plants reach sulphur deficiency, as they do in the field, but they don’t die. In other words, we applied mild sulphur stress, because at high stress, plants won’t flower at all. There is no linear response between S availability and the observed problems, we don’t know what the exact thresholds are.”

Brassica rapa flowers, (left) with enough sulphur and (right) without enough sulphur. Credit Ausma et al. 2021.

What does an unhappy plant look like? If it has yellow flowers, then without sulphur, those flowers are paler. Even if they don’t rely on yellow pigment, things go badly without sulphur. The flowers are smaller and more likely to be strangely shaped. The flowers might not look right to us, but human opinion doesn’t matter too much. Instead, it’s what the pollinators see that matters and the team also used vision modelling to find out. They discovered that the insect would see much smaller and much less colourful yellow flowers. That’s important because it’s a signal the plant sends to the pollinator.

Ausma and colleagues refer back to Schnug and Haneklaus, who found that, after pollination, B. rapa flowers fade and shrink to become less visible to bees. That way, the plant can direct the bees to the flowers that need pollinating and away from the flowers that are now busy forming seeds. Ausma and colleagues point out that if some B. rapa flowers are pre-shrunk and faded, they’re going to confuse the target audience. 

You can also see an effect on pollen in B. rapa. The quantity of pollen is the same, but the size is a lot smaller. Ausma and colleagues argue that in addition to sulphur-deprived flowers being less effective, so too is the pollen within them, compounding the effect of sulphur deprivation. This can also knock on to the pollinators, write the botanists. “Pollinators require a specific ratio of mineral nutrients in their (pollen) food… and sulphur deprivation affected these ratios in pollen, since it drastically decreased the pollen sulphur and potassium content across different species… Experiments with Osmia bicornis demonstrated that bee fitness is particularly affected by low amounts of minerals – including potassium (Filipiak, 2019) – suggesting that sulphur deprivation indeed negatively affects pollinators.”

If sulphur deficiency is such a problem, another puzzle is why are people looking at it now, and not sooner? One possible answer is that the world is a better place than it was, causing problems for some plants. In particular, there’s a lot less acid rain. Emissions of sulphur dioxide would react with water to add sulphuric acid to create acid rain. In his email, van der Kooi writes, “Due to the disappearance of acid rain, the S concentration around plants is lower. This is beneficial for a lot of reasons, particularly in nature reserves, but some crop species, particularly Brassica spp that need a lot of S, can suffer. Currently, in the western world, there is almost no S left in our atmosphere.”

Luit De Kok, one of the co-authors, was also a co-author on another paper that tackled this problem. That paper by Tahereh Aghajanzadeh and colleagues found that Brassica juncea and Brassica rapa could use H2S and SO2 absorbed through the leaves.

It raises the possibility that one reason sulphur has been overlooked is that we’ve been adding it extensively in the past without noticing. How much? A staggering fact in Ausma and colleagues’ paper is that as much as 50% of Germany’s forests may suffer from a lack of sulphur. They also have evidence that 50% of agricultural land in the USA is sulphur deficient and cite research showing how sulphur fertilisation can help boost seed yield in the UK.

While this might look like an agricultural problem, Ausma and colleagues write in their conclusion that there’s a lot more interest beyond humans in the crops in the fields. “[O]ur study paves the way for studies on how sulphur deprivation affects the fitness of plants, pollinators and organisms at different trophic levels, so to eventually obtain a better understanding of the bottom-up impact of nutrient deficiency on whole (agro-)ecosystem functioning.”

RESEARCH ARTICLE

Ausma, T., Bansal, V., Kraaij, M., Verloop, A.C.M., Gasperl, A., Müller, M., Kopriva, S., De Kok, L.J., van der Kooi, C.J., 2021. Floral displays suffer from sulphur deprivation. Environmental and Experimental Botany. https://doi.org/10.1016/j.envexpbot.2021.104656

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