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BOTANY

Underground strategies

Root specializations enable plants to live in impoverished environments like Brazil’s rupestrian grasslands

Typical rupestrian grassland landscape in the Canastra Mountains

RAFAEL OLIVEIRATypical rupestrian grassland landscape in the Canastra MountainsRAFAEL OLIVEIRA

When they went off to the Serra do Cabral Mountains in the state of Minas Gerais to examine the vegetation with a botanist’s eye, biologist Rafael Oliveira of the University of Campinas (Unicamp) and his students were prepared for surprises. In this environment, where plants grow on rocks or in the midst of sand so white it looks like salt—hence known as rupestrian grassland (campo rupestre)—it is surprising that they find ways to survive. But they succeed, thanks to an arsenal of tricks that researchers have only just begun to identify. And the variety of tricks is surprising as well. A yet-to-be-published survey headed by biologist Fernando Silveira of the Federal University of Minas Gerais estimates that there are some 11,000 species (one-third of Brazil’s plant biodiversity) in an area that makes up less than 1% of the country’s landmass, scattered mainly throughout the Serra do Espinhaço Mountains. “We are still a long way from understanding the evolutionary mechanisms that generate and maintain such diversity,” says Oliveira, who participated in the survey.

At first glance, the Unicamp team noticed that only four species were commonly found in these sandy areas of water- and nutrient-impoverished soil, and that one species nearly always appeared close to a different plant, among other findings. “There must have been something special that enabled this coexistence,” Oliveira recalls. One such solution, commonly found in rupestrian grasslands, is to be carnivorous. The delicate Philcoxia minensis keeps its tiny, sticky leaves buried in the sand, where it captures and digests nematodes, as shown in a 2012 paper published in the journal PNAS, which was the product of the undergraduate research of biologist Caio Pereira (see Pesquisa FAPESP Issue No. 194). It is the first time anyone has identified the ability to consume animals in a species of the family Plantaginaceae, and hence the discovery broadens the scope of this strategy. But the landscape held further novelties. When they dug up cacti of the species Discocactus placentiformis, a spiny sphere that leaves only a piece of its top exposed, they saw curious-looking roots coated with fine sand. “Even when we washed them, the sand did not come off,” Oliveira says.

An investigation of the substance released by these roots, and the role it plays, was the subject of the master’s thesis of Anna Abrahão. Her work called for a rather unorthodox solution: hydroponic cultivation in the greenhouse of the Functional Plant Ecology Laboratory coordinated by Oliveira. The idea of keeping plant roots submerged in water when they normally receive scarcely any water at all was considered dubious by colleagues, but it was the only way to control the amount of nutrients available. “In soil, we never know how much is available to the plant, because the substances form compounds that don’t break down easily,” the biologist explains.

In a further surprise, the excess water did not turn out to be a problem, but the amount of nutrients was a more critical factor than they had imagined. In an earlier attempt to grow rupestrian grassland plants in the laboratory, Oliveira diluted commercial fertilizer by half to account for the dearth of nutrients in the natural habitat where they live. All of them were poisoned by the excess and died. “We were not successful until the nutrient compound was one-tenth of the original concentration.”

Through the practice of keeping the roots uncovered, it was possible to see the formation of clusters of root hairs that secrete substances known as carboxylates and keep the sand clinging to them. The carboxylates break down the phosphorous, aluminum and iron compounds present in the sand that are unavailable to the plants in that form. In this way, they are able to absorb phosphorous, which is essential for vital functions (such as photosynthesis and building genetic material) and is scarce in the quartz-based soil. “This secretion is an impressive innovation,” Oliveira explains. “It chemically manipulates the soil; other plants cannot survive under these conditions.”

Fog: source of moisture

RAFAEL OLIVEIRAFog: source of moistureRAFAEL OLIVEIRA

The roots are thus able to mobilize not only phosphorous, but also other micronutrients that are important for development and growth. These substances are so rare in such soils that it becomes difficult to detect them by customary means. Manganese, however, has proven to be more common in the leaves of species with root specializations, enough so to make it a potential indicator of this type of strategy, according to a February 2015 paper in the journal Trends in Plant Science.

An experiment with cacti, from which the findings were published in October 2014 in the journal Oecologia, also showed that when there is more phosphorous in the soil, the roots respond by producing fewer carboxylates. “The plants have a set of strategies on a very small scale, with adaptive solutions more diverse than we had imagined,” the Unicamp researcher notes.

The discovery that Discocactus use this strategy to obtain nutrients was also surprising because the cactus family is known for forming associations with fungi on their roots, known as mycorrhizas, which transfer phosphorus to the plant and take up carbon from it. “The publisher of the article thought this was impossible, since it is a mycorrhizal family,” Oliveira recalls. In his view, it is an indication of how these plants’ diverse arsenal of tricks is largely ignored, particularly under the extreme conditions of the rupestrian grasslands, which are still not well-known throughout the world.

Strawflower: Actinocephalus polyanthus

RAFAEL OLIVEIRAStrawflower: Actinocephalus polyanthusRAFAEL OLIVEIRA

His research on this region has enabled Oliveira to test a theoretical model developed by Hans Lambers, a Dutch biologist based at the University of Western Australia. In a 2008 paper published in the journal Trends in Ecology and Evolution, Lambers showed that in ancient nitrogen- and phosphorus-impoverished soils, mycorrhizas are not the most common strategy. In these environments, phosphorus is a stronger limitation than nitrogen, in contrast to what occurs in younger soils. Instead, root modifications such as clusters of hairs and carboxylate secretion are believed to appear. The suggestion is based on studies carried out in two regions having characteristics very similar to those of the rupestrian grasslands: the fynbos of South Africa, and the kwongan of southwestern Australia. Fascinated with the paper, Oliveira, who was beginning a project to evaluate the water-acquisition strategies of rupestrian grassland plants, took the opportunity to include nutrients in his studies.

In so doing, Oliveira carried out the first test of Lambers’ theory, and in the process, Lambers was captivated by the rupestrian grasslands and began a research partnership with the Unicamp group, where he will teach month-long courses on a visiting basis over the next three years. An analysis of soil from the Serra do Cabral Mountains and of 50 of that area’s most important plant species indicates that the rupestrian grassland is indeed similar to the fynbos and the kwongan in terms of scarcity of nutrients, particularly phosphorus. They are also similar in the way the plants acquire nutrients more commonly through root specializations than through mycorrhizal association, as shown in a paper that resulted from the master’s thesis of Hugo Galvão, published in New Phytologist in February 2015.

Almas Peak, in Bahia

RAFAEL OLIVEIRAAlmas Peak, in BahiaRAFAEL OLIVEIRA

An observation made by research intern Ana Luíza Muler on trips to the mountains in Minas Gerais also yielded an independent test. During a period she spent in Australia, she studied two plants that usually coexist in close proximity, as is the case for a species from the Iridaceae family that is usually associated with a strawflower in the Serra do Cabral Mountains. The plants in Australia were Banksia attenuata, whose roots form clusters that release carboxylates and acquire phosphorus from the soil, and Scholtzia involucrata, which has no specialization. In an experiment discussed in a 2014 paper in Oecologia, she showed that this second plant grows better when the other species is present, suggesting that it uses the nutrients made available through the chemical alternation of the soil. To what extent this occurs and how these different plants coexist are yet to be investigated.

The parallels between the continents are a vestige of a very distant past in which they were positioned close together on the supercontinent Gondwana. The plant families at the center of these discoveries are largely representatives of families that existed during that long-ago time: the Proteaceae, whose specialized roots, familiar on other continents, led Oliveira’s group to look for similarities here, and the Velloziaceae (tree-lilies) and Eriocaulaceae (strawflowers), both of which are more diversified in Brazil than elsewhere. The secrets they conceal in the sand promise to show that the mechanisms well known in tropical forests are not the rule, and they place the rupestrian grasslands at the forefront of this new understanding of how plants are able to manage in extreme situations.

Project
Climate change in Brazilian mountains: functional responses of native plants from campos rupestres and campos de altitude to extreme droughts (No. 12/07271-7); Grant mechanism Regular Line of Research Project Award; Principal Investigator Rafael Silva Oliveira (Unicamp); Investment R$569,639.14 (FAPESP).

Scientific articles
ABRAHÃO, A. et al. Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus. Oecologia. V. 176, No. 2, p. 345-55. Oct. 2014.
LAMBERS, H. et al. Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends in Plant Science. V. 20, No. 2, p. 83-90. Feb. 2015.
MULER, A. L. et al. Does cluster-root activity benefit nutrient uptake and growth of co-existing species? Oecologia. V. 174, No. 1, p. 23-Jan. 31, 2014.
OLIVEIRA, R. S. et al. Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytologist. V. 205, No. 3, p. 1183-94. Feb. 2015.
PEREIRA, C. G. et al. Underground leaves of Philcoxia trap and digest nematodes. PNAS. V. 109, No. 4, p. 1154-8. Jan. 24, 2012.

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