Science & Society Plants, climate and humans Plant intelligence changes everything Frantisek Baluska1 & Stefano Mancuso2 lobal climate change is among the important organisms on Earth. Among all Around 30% of all organic compounds most urgent problems that science multicellular organisms, only plants have generated via photosynthesis are released G has to deal with in the 21st century. the ability to convert sunlight into organic from root apices either as exudates [3] or Scientists have developed ever more substances via photosynthesis and are as sugars to feed symbiotic fungi [4] in complex models in order to understand the therefore able to live a more or less inde- exchange for water, phosphate, nitrate and driving factors of climate change and to pendent life, whereas all other organisms, critical minerals (Fig 1). Exudates released predict future scenarios. Yet, for all their including humans, fully depend on plants into the rhizosphere also attract or repel sophistication, these models might over- as primary producers of both food and microorganism to maintain the root micro- look a crucial factor with potentially enor- oxygen. Moreover, most plants—perhaps biome, and shape the physico-chemical mous implications for predicting and with the few crop plant exceptions such as properties of the soil [3]. In particular, root dealing with climate change as they maize—would likely be able to survive if exudates and mucilages induce biotic soil consider usually plants only as passive the humankind vanished. The opposite is aggregation which is important for carbon elements that convert atmospheric CO2 into clearly not true, unless we will develop stabilization within soil. Organic soil is not biomass. However, over the past decades, novel efficient technologies of artificial just the result of physical weathering rock plant science has revealed that higher photosynthesis to convert solar energy into and stones, but of the coordinated biologi- plants are much more than just passive organic matter. cal activities of fungi, bacteria and plant carbon-fixing entities. They possess a ...................................................... roots. Moreover, the large amounts of plant-specific intelligence, with which they organic substances that flow from the roots manipulate both their abiotic and biotic “The fact that plant roots to the microbiota generate huge networks environment, including climate patterns actively control carbon in via fungal hyphae that interconnect numer- and whole ecosystems. Considering plants ous plants and plant species into supra- as active and intelligent agents has there- the soil, further supports the organismal networks [3]. The fact that fore profound consequences not just for view that plants may also be plant roots actively control carbon in the future climate scenarios but also for under- able to actively control soil further supports the view that plants standing mankind’s role and position climate.” may also be able to actively control within the Earth’s biosphere. ...................................................... climate [3]. ...................................................... ...................................................... “ When the first ancestors of terrestrial Considering plants as active plants left the oceans to colonize the land, “Our tight co-evolution and intelligent agents has they joined fungi and bacteria to transform and the reliance of humans therefore profound rocks and deserts into green ecosystems on plants to provide food, consequences not just for teeming with life. Ever since, they have been playing a crucial role in generating and medicines and recreational future climate scenarios but maintaining the climatic conditions neces- drugs might raise the question also for understanding sary to support terrestrial life [1,2]. Above of who actually domesticated mankind’s role and position the Earth’s surface, photosynthetic leaf cells whom.” within the Earth’s biosphere.” and tissues generate complex organic ...................................................... ...................................................... compounds from carbon dioxide and release oxygen into the atmosphere. Under the Plants release also huge amounts of Autotrophic plants as primary organisms Earth’s surface, plant roots shape and main- carbon-based volatiles into the Earth’s atmo- tain the soil, a carbon-based ecosystem that sphere. These compounds are involved in In terms of global carbon flux and food provides a unique biosphere for microbial plant–plant communication, as well as chains, autoptrophic plants are the most and fungal organisms. manipulation of their biotic and abiotic 1 University of Bonn, Bonn, Germany. E-mail: [email protected] 2 University of Firenze, Firenze, Italy. E-mail: [email protected] DOI 10.15252/embr.202050109 | EMBO Reports (2020) 21:e50109 | Published online 27 February 2020 ª 2020 The Authors. Published under the terms of the CC BY NC ND 4.0 license EMBO reports 21:e50109 | 2020 1 of 5 EMBO reports Frantisek Baluska & Stefano Mancuso environments, also by attracting or repelling insects and other organisms. By way of example, trees annually produce around 500 Gt of the highly reactive gas isoprene, along Fungal Transition Rhizobia bacterial symbiosis zone symbiosis with large amounts of monoterpenes, sesquiterpenes and other biogenic volatile compounds. We still know very little about the biological role and mechanism of this Volatiles Root exudates chemical communication, but it is very likely that this huge amount of volatiles affects the composition of the atmosphere Apical (Fig 2). meristem Bacterial Co-evolution symbiosis The oldest mycorrhiza-root fossils are some — Root Released 450 million years old from the very begin- Mucilage cap root cap cells ning when ancient plants populated the land [5]. This fact shows that mycorrhizal symbi- © EMBO © otic fungi co-evolved with the emerging roots of the ancient plants and that their Figure 1. Functional organization of plant root apex. tight association was essential for success- The root apex actively releases carbon via several different pathways. Root cap cells secrete mucilage which fully colonizing a barren and hostile land facilitates root growth within soil. Peripheral root cap cells are released in large amounts; these cells often [1]. Nowadays, many mycorrhizal fungi are continue to live in, and actively manipulate, the rhizosphere. For example, root apices of Gossypium hirsutum shed up 10,000 cells in 24 h. Root apices also compound for manipulating the biotic and biotic rhizosphere so tightly integrated with plant roots that environment as well as carbon-based volatiles and info-chemicals. Finally, root apices also provide large they are no longer able to exist or proliferate amounts of sucrose and lipids to feed their symbiotic fungal partners. The sheer abundance of root apices in the independently: their spores germinate only soil biosphere makes the plant root apex one of the most important plant organs. if roots are close enough to invade their Infochemicals Fungal symbionts Nutrients Bacterial symbionts FUNGAL NETWORK Root exudates Soil microbes Volatiles © EMBO © Figure 2. Root-fungal-microbial integrated networks. Neighbouring plants communicate through their roots via exudates and volatile info-chemicals. Root apices also communicate with mycorrhiza fungi and organize integrated root-fungal networks. More than 90% of all plants, from liverworts up to angiosperms, form these symbiotic networks, which improve plant nutrition via providing plants with water and critical nutrients. These symbiotic fungi also improve plant performance under stress and allow plants to share messages and signals with neighbouring plants. 2 of 5 EMBO reports 21:e50109 | 2020 ª 2020 The Authors Frantisek Baluska & Stefano Mancuso EMBO reports tissues. Intriguingly, mycelial networks their pollinators and bodyguards. Our tight needs [7–10] could therefore dramatically demonstrate goal-directed, memory-based co-evolution and the reliance of humans on change our understanding of life on Earth behaviour related to foraging with implica- plants to provide food, medicines and recre- and help us to better cope with climate tions for carbon distribution in forest soils ational drugs might raise the question of changes. Better understanding of plant intel- [4]. It seems that this behaviour of who actually domesticated whom [7,8]. ligence is relevant not only for maintaining mycorrhizal fungi may assist plant roots to A new view of higher plants as cognitive life-supporting ecosystems and climate explore soils in their search for water and and intelligent organisms that actively patterns, but also for understanding their co- minerals. manipulate their environment to serve their evolution with insects and animals, as well All this means that plants are not just passive organisms that merely sit around and sequester CO2 from the atmosphere until they are eaten. In contrast, plants display highly goal-oriented behaviour by constantly assessing and manipulating their environment to fit it to their needs. A strik- ing example of this manipulation is the reproductive strategies of many flowering plants that rely on insects, birds or small mammals to distribute their pollen or seeds. Plants actively control these pollinators by attracting them using not only nectar as a food reward but also by manipulating the behaviour of insect pollinators via brain- altering chemicals [6]. This manipulation of animals achieves