How do plants defend themselves from root-eating creatures?

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PLANTS: SURVIVING IN A DANGEROUS WORLD

Plants are an important food source for many creatures, includi ng humans. Plant eaters, or herbivores, can be large mammals like cows,HERBIVORE An animal that eats plants. sheep, or horses, but most of them are actually much tinier, such as caterpillars or aphids (Figure /one.tnum). Because these tiny herbivores usually occur in large numbers, they can cause a lot of damage. Insects, for example, are the most diverse group of animals on Earth. The re are around /one.tnum million known species of insects, of which about half are herbivores. In comparison, there are only around /five.tnum,5zero.tnum/zero.tnum mammal species living on Earth. In addition to the large and small herbiv ores aboveground, there are many plant feeders living belowgroundas well. The soil is ﬁlled with many kinds of herbivores that feed on plant roots, including insect larvae, tiny worms called nematodes, and spider-like NEMATODES Tiny, wormlike animals that mostly occur in the soil, but also in seas or lakes, in the intestines of animals, and even in the guts of insects. creatures called mites (Figure /one.tnum). There are usually high numbers of herbivores present in the so il, just like there are aboveground. For example, there are 3zero.tnum,0zero.tnum/zero.tnum known nematodes species, of which around 1zero.tnum% are plant eaters. One single female nematode produces up to 2zero.tnum/zero.tnum eggs. This means that a single plant can be attacked by thousands of nematodes at the same time. Chewing insects are another danger. They may chew through the water transport system of plant roots, which can cause the leaves to droop and the plant to die from lack of water.

HOW DO PLANTS DEFEND THEMSELVES?

With so many creatures trying to attack them, you can imagine that plants have a hard time surviving. Since plants cannot ﬂee from th eir attackers, they had to evolve ways of defending themselves. Plants have developed several defenses against herbivores [/one.tnum]. Some plant defenses are easy to see, like the thorns of a rose, the hairs on the PLANT DEFENSES Features of a plant that aﬀect the behavior, growth, or survival of herbivores. leaf of a stinging nettle, or the thick skin of beetroots. Other defens es, such as chemical defenses, are less visible. Each plant prod uces thousands of diﬀerent chemicals, all involved in essential pr ocesses. Some chemicals, like sugars, provide energy to the plant. Other groups of chemicals help to defend plants against attackers. These chem ical defenses can make the plant taste bad, which prevents herbivores from eating plant tissues. In some cases, the chemicals can even be tox ic. Chemical defenses can aﬀect humans too. There are many plants tha t would make you feel very sick if you ate them, for example the berri es of black nightshade. Some plants, such as poison ivy or hogweed, can give you a rash and even cause burns when you touch them. Most chemical defenses are not that bad, though. In fact, chances are high that you have been exposed to plant chemical defenses yourself . We have grown to like the taste of some chemicals that plants produce. Have you ever put mustard on your hotdog or sausage, or enjoyed a nice Indian curry with mustard seeds? The sharp-bitter taste of mustard is caused by defense chemicals called glucosinolates. In the GLUCOSINOLATES Defense substances responsible for the sharp bitter taste of mustard and wasabi. Although most humans enjoy their taste, they are toxic to most insects, nematodes and bacteria. wild, glucosinolates help plants to defend themselves against in sects, fungi, and bacteria. The caﬀeine in coﬀee, which helps people to wake up in the morning, is not made by coﬀee trees to please humans. In reality, coﬀee trees produce caﬀeine to protect their seeds—the coﬀee beans—from insect attacks. Caﬀeine not only gives coﬀee beans their bitter taste, but it can also paralyze or kill insects try ing to feed on them. These examples illustrate that chemical defenses are an eﬀectiv e way for plants to protect themselves against herbivores in their environments. Nevertheless, most plants are not completely defended by these chemicals. If you take a good look at the plants around you, you will notice that most plants show some damage, such as holes in their leaves. This is because the production of chemica l defenses comes at a cost. Plants do not only have to worry about defending themselves, but they must also put energy into growth, producing ﬂowers, and making seeds. So, the energy plants can sp end on producing defenses is limited. Plants must make use of this li mited amount of energy in an eﬃcient way.

HOW DO PLANTS DEFEND THEMSELVES EFFICIENTLY?

Fossils of herbivore-damaged leaves show that plants and herb ivores have been living together on Earth for more than 4zero.tnum/zero.tnum million years. During this time, plants have developed several ways to produce defenses in a cost-eﬃcient manner. One way is to produce defense s only when necessary, for example, when insects start eating them [/two.tnum]. By only producing defenses when under attack, plants save energy when no dangers are present. The disadvantage of this strategy is tha t defense production will only begin after the herbivore starts eatin g. Because defense production takes time, the plant can suﬀer signiﬁcant damage before the herbivore leaves or dies. Another strategy is to always have some defenses at hand but in limited amounts. In this case, the plant moves most defenses to the plant parts that are most important for survival and are vulnerable to attack b y herbivores [/three.tnum]. This would be like defending a castle by putting the soldiers on the outer wall, where the ﬁrst attack would occur and where the castle is most vulnerable. Clearly, the treasure in the cas tle would be well guarded too, as this is the most valuable. Abovegroun d, such valuable plant parts include young leaves, ﬂowers, and se eds, which play essential roles in energy production or in producing the next generation. Belowground, various parts of the root system also have diﬀerent values. The root systems of plants like tomato or cabbage consist of three parts: the taproot, lateral roots, and ﬁne roots (Figure /two.tnum). TAPROOT Main root from which lateral roots arise. Collects water and nutrients from the rest of the root system and distributes them aboveground. In carrots and beetroots, it stores starch and nutrients. Lateral and ﬁne roots help the plant take up valuable nutrients and water from the soil. The taproot is the main root that collects all the water and nutrients absorbed by the lateral and ﬁne roots and distributes them to the aboveground parts. Simultaneously, sugars and other substances produced in the leaves move through the taproot in the other direction. The important role of the taproot in transpor t of nutrients and water makes it an essential part of the root system. When herbivores damage the taproot, the essential transport routes are broken, and the plant will die. In plants like beets, the taproot stores energy in the form of sugar. This is like the treasure in the castle. The taproot is therefore considered the most valuable ro ot part and is defended the most, followed by the lateral and ﬁne roots [/four.tnum] (Figure /two.tnum).

HOW DO PLANT DEFENSES AFFECT SOIL HERBIVORES?

Herbivores decide which root part to eat based both on its nutrition al value and on how well it is defended [/five.tnum]. Most herbivores would prefer to feed on the taproot since it is the most nutritious part of the root system. However, as mentioned earlier, the taproot is also the best-defended part. Not all herbivores can overcome these chem ical defenses. Some herbivores, like the larvae of the cabbage root ﬂy, can deactivate chemical defenses and feed on the taproot [/four.tnum]. Other herbivores, like the larvae of the European June beetle, cannot d eal with the high defense levels in the taproot and instead eat the lateral and ﬁne roots (Figure /two.tnum). The distribution of chemical defensesacross the root system and the ability of herbivores to overcome these defenses can therefore have a strong inﬂuence on where herbivor es can be found in the soil.

HOW CAN SCIENTISTS USE THIS KNOWLEDGE?

The knowledge gained by studying the defense systems of plants helps us to understand how plants interact with herbivores and other The distribution of chemical defenses over a root system, and how this aﬀects belowground herbivores. Red indicates the highest defense level in the root system and yellow indicates the lowest level. Chemical defenses are generally highest in the taproot (red), followed by the lateral roots (orange) and the ﬁne roots (yellow). Some insect herbivores, like the cabbage root ﬂy, can deactivate a plant’s chemical defenses and can eat the taproot where defenses are highest. Other herbivores, like the European June beetle, cannot deactivate plant defenses and therefore they eat the ﬁne roots, where chemical defense levels are lower. (Image credit: Jennifer Gabriel). animals in their environments. In addition, knowing how plants de fend themselves can help us to develop more environmentally friendly ways of growing crops. Plant breeding can create new crop varieties, such PLANT BREEDING The science of creating new plant varieties with desirable characteristics like taste, smell, color, or resistance to herbivores or certain environmental conditions like drought. as plants with nicer colors, more interesting tastes, or bigger frui ts. Similarly, plant breeders can create crops that are better defen ded against attackers. To do so, plant breeders must understand howplants produce defenses, and which attackers those defenses are eﬀectiv e against. Scientists who study plant defenses using lab experimen ts and ﬁeld studies collect this kind of information. By creating cr ops with better defenses, we can help farmers to reduce the amounts of chemical pesticides they use. This is good news for both human health and the health of our environment. ACKNOWLEDGMENTS We thank Jennifer Gabriel (iDiv, Leipzig) for her great help with the ﬁgures. We are grateful for the support from the editors of the Soil Biodiversity collection during the writing process and for the kin d remarks of the young reviewers and their mentors whose advice was essential for the completion of this paper. Finally, we would lik e to thank the German Research Foundation (DFG) for funding our research on cabbage root ﬂies at iDiv (DFG–FZT 1one.tnum/eight.tnum, 2zero.tnum2five.tnum4eight.tnum8one.tnum/six.tnum), in collaboration with ChemBioSys (SFB 1one.tnum2seven.tnum, 2three.tnum9seven.tnum4eight.tnum5two.tnum/two.tnum). REFERENCES /one.tnum. Ehrlich, P . R., and Raven, P . H. 1nine.tnum6four.tnum. Butterﬂies and plants-a study in coevolution. Evolution. 1eight.tnum:5eight.tnum/six.tnum–6zero.tnum/eight.tnum. /two.tnum. Karban, R. 2zero.tnum2zero.tnum. The ecology and evolution of induced responses to herbivory and how plants perceive risk. Ecol. Entomol. 4five.tnum:/one.tnum–/nine.tnum. doi: 1zero.tnum.1one.tnum1one.tnum/een.1two.tnum7seven.tnum/one.tnum /three.tnum. Meldau, S., Erb, M., and Baldwin, I. T. 2zero.tnum1two.tnum. Defence on demand: mechanisms behind optimal defence patterns. Ann. Bot. 1one.tnum/zero.tnum:1five.tnum0three.tnum–1four.tnum. doi: 1zero.tnum.1zero.tnum9three.tnum/aob/mcs2one.tnum/two.tnum /four.tnum. Tsunoda, T., Grosser, K., and van Dam, N. M. 2zero.tnum1eight.tnum. Locally andsystemically induced glucosinolates follow optimal defence allocation theo ry upon root herbivory. Funct. Ecol. 3two.tnum:2one.tnum2seven.tnum–3seven.tnum. doi: 1zero.tnum.1one.tnum1one.tnum/1three.tnum6five.tnum-2four.tnum3five.tnum.1three.tnum1four.tnum/seven.tnum /five.tnum. Tsunoda, T., and van Dam, N. M. 2zero.tnum1seven.tnum. Root chemical traits and their roles in belowground biotic interactions. Pedobiologia (Jena). 6five.tnum:5eight.tnum–6seven.tnum. doi: 1zero.tnum.1zero.tnum1six.tnum/j.pedobi.2zero.tnum1seven.tnum.0five.tnum.0zero.tnum/seven.tnum SUBMITTED: 2nine.tnum January 2zero.tnum2one.tnum;ACCEPTED: 2eight.tnum March 2zero.tnum2two.tnum; PUBLISHED ONLINE: 2five.tnum April 2zero.tnum2two.tnum. EDITOR: Helen Phillips, Saint Mary’s University, Canada SCIENCE MENTORS: Ryan Thomas Weir and Ruchira Sharma CITATION: Touw AJ and van Dam NM (2zero.tnum2two.tnum) How Do Plants Defend Themselves From Root-Eating Creatures? Front. Young Minds 1zero.tnum:6six.tnum0seven.tnum0one.tnum. doi: 1zero.tnum.3three.tnum8nine.tnum/frym. 2zero.tnum2two.tnum.6six.tnum0seven.tnum0one.tnum CONFLICT OF INTEREST: The authors declare that the research was conducted in the absence of any commercial or ﬁnancial relationships that coul d be construed as a potential conﬂict of interest. COPYRIGHT © 2zero.tnum2two.tnum Touw and van Dam. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided th e original author(s) and the copyright owner(s) are credited and that the or iginal publication in this journal is cited, in accordance with accepted academic prac tice. No use, distribution or reproduction is permitted which does not comply with t hese terms. YOUNG REVIEWERS AVANI, AGE: 1zero.tnum Hello, I am Avani. I enjoy running and swimming. I am also a dancer . I love going on walks with my dog, or collecting stones. I love math, science and I love sports. I enjoy playing video games, and calling friends. I love nature and cold windy weather. CATHERINE, AGE: 1five.tnum I love music and singing, I play the violin and guitar and I also e njoy writing! I am part of a highland dance troup and volunteer with children at loc al kids clubs and guides. I enjoy attending youth events at my church and doing ﬁtnes s. I hope that by reviewing these articles I could learn about new and interes ting stuﬀ! HARRISON, AGE: 1one.tnum I love playing sports such as hockey and go running and chasing my dog! I also love discovering new things, but not new food! Because I currently go t o primary school I am excited to start my new secondary school and try lots of new subjects. My favorite subject at the minute is maths. AUTHORS AXEL J. TOUW Axel has been fascinated by nature since he was young. At that ti me, he was mostly interested in dinosaurs, cats, dogs, lizards, and frogs, but particularly in birds. Actually, the ﬁrst thing he ever drew was an owl (with some imagination). Whil e studying biology, he became interested in how plants communicate, especiall y with insects. Today, Axel studies how plants defend themselves against microbes,nematodes, and insects. In his free time, he likes to be outside, play football, re ad, and cook. He also tries to use the knowledge gained during his research in his gar den, with varying degrees of success. *[email protected] NICOLE M. VAN DAM Nicole was born and grew up in the Netherlands with her parents an d two younger sisters. As a kid, she liked to experiment with insects. For example, she tested whether ants can swim by putting them in puddles (in case you are wondering, th ey do quite well). She studied biology in Wageningen, the Netherlands . There she became interested in how plants can defend themselves and how farmers ca n use this knowledge to reduce pesticide use. After doing a lot more experiments with insects and plants in various places in the world, she became a professor. In her free time, she likes to do yoga and to watch movies with her two sons (1nine.tnum and 2one.tnum). Together with her husband, she likes to grow organic fruits and vegetables in her garden. There she also ﬁnds inspiration for new research projects.