There has been a dramatic recent increase in the understanding of the mechanisms by which plants detect their neighbors,(1) including by touch,(2) reflected light,(3) volatile organic chemicals, and root exudates.(4,5) The importance of root exudates remains ill-defined because of confounding experimental variables(6,7) and difficulties disentangling neighbor detection in shoot and roots.(8-10) There is evidence that root exudates allow distinction between kin and non-kin neighbors,(11-13) but identification of specific exudates that function in neighbor detection and/or kin recognition remain elusive.(1) Strigolactones (SLs), which are exuded into the soil in significant quantities in flowering plants to promote recruitment of arbuscular mycorrhizal fungi (AMF),(14) seem intuitive candidates to act as plant-plant signals, since they also act as hormones in plants,(15-17) with dramatic effects on shoot growth(18,19) and milder effects on root development.(20) Here, using pea, we test whether SLs act as either cues or signals for neighbor detection. We show that peas detect neighbors early in the life cycle through their root systems, resulting in strong changes in shoot biomass and branching, and that this requires SL biosynthesis. We demonstrate that uptake and detection of SLs exuded by neighboring plants are needed for this early neighbor detection, and that plants that cannot exude SLs are outcompeted by neighboring plants and fail to adjust growth to their soil volume. We conclude that plants both exude SLs as signals to modulate neighbor growth and detect environmental SLs as a cue for neighbor presence; collectively, this allows plants to proactively adjust their shoot growth according to neighbor density.

Vascular plants, unlike bryophytes, have a strong root-shoot dichotomy in which the tissue systems are mutually interdependent; roots are completely dependent on shoots for photosynthetic sugars, and shoots are completely dependent on roots for water and mineral nutrients. Long-distance communication between shoot and root is therefore critical for the growth, development and survival of vascular plants, especially with regard to variable environmental conditions. However, this long-distance signalling does not appear an ancestral feature of land plants, and has likely arisen in vascular plants to service the radical alterations in body-plan seen in this taxon. In this review, we examine the defined hormonal root-to-shoot and shoot-to-root signalling pathways that coordinate the growth of vascular plants, with a particular view to understanding how these pathways may have evolved. We highlight the completely divergent roles of isopentenyl-adenine and trans-zeatin cytokinin species in long-distance signalling, and ask whether cytokinin can really be considered as a single class of hormones in the light of recent research. We also discuss the puzzlingly sparse evidence for auxin as a shoot-to-root signal, the evolutionary re-purposing of strigolactones and gibberellins as hormonal signals, and speculate on the possible role of sugars as long-distance signals. We conclude by discussing the 'design principles' of long-distance signalling in vascular plants.

The production of seed in flowering plants is complicated by the need to first invest in reproductive shoots, inflorescences, flowers, and fruit. Furthermore, in many species, it will be months between plants generating flowers and setting seed. How can plants therefore produce an optimal seed-set relative to environmental resources when the “reproductive architecture” that supports seed-set needs to be elaborated so far in advance? Here, we address this question by investigating the spatio-temporal control of reproductive architecture in Arabidopsis (Arabidopsis thaliana) and Brassica napus. We show that resource and resource-related signals such as substrate volume play a key role in determining the scale of reproductive effort, and that this is reflected in the earliest events in reproductive development, which broadly predict the subsequent reproductive effort. We show that a series of negative feedbacks both within and between developmental stages prevent plants from over-committing to early stages of development. These feedbacks create a highly plastic, homeostatic system in which additional organs can be produced in the case of reproductive failure elsewhere in the system. We propose that these feedbacks represent an “integrated dominance” mechanism that allows resource use to be correctly sequenced between developmental stages to optimize seed set.

Vascular plants, unlike bryophytes, have a strong root-shoot dichotomy in which the tissue systems are mutually interdependent; roots are completely dependent on shoots for photosynthetic sugars, and shoots are completely dependent on roots for water and mineral nutrients. Long-distance communication between shoot and root is therefore critical for the growth, development and survival of vascular plants, especially with regard to variable environmental conditions. However, this long-distance signalling does not appear an ancestral feature of land plants, and has likely arisen in vascular plants to service the radical alterations in body-plan seen in this taxon. In this review, we examine the defined hormonal root-to-shoot and shoot-to-root signalling pathways that coordinate the growth of vascular plants, with a particular view to understanding how these pathways may have evolved. We highlight the completely divergent roles of isopentenyl-adenine and trans-zeatin cytokinin species in long-distance signalling, and ask whether cytokinin can really be considered as a single class of hormones in the light of recent research. We also discuss the puzzlingly sparse evidence for auxin as a shoot-to-root signal, the evolutionary re-purposing of strigolactones and gibberellins as hormonal signals, and speculate on the possible role of sugars as long-distance signals. We conclude by discussing the ‘design principles’ of long-distance signalling in vascular plants.

Plants must carefully coordinate their growth and development with respect to prevailing environmental conditions. To do this, plants can use a range of nutritional and non-nutritional information that allows them to proactively modulate their growth to avoid resource limitations. As is well-known to gardeners and horticulturists alike, substrate volume strongly influences plant growth, and maybe a key source of non-nutritional information for plants. However, the mechanisms by which these substrate volume effects occur remain unclear. Here, we show that wheat plants proactively modulate their shoot growth with respect to substrate volume, independent of nutrient availability. We show that these effects occur in two phases; in the first phase, the dilution of a mobile 'substrate volume-sensing signal' (SVS) allows plants to match their shoot (but not root) growth to the total size of the substrate, irrespective of how much of this they can occupy with their roots. In the second phase, the dilution of a less mobile 'root density-sensing signal' (RDS) allows plants to match root growth to actual rooting volume, with corresponding effects on shoot growth. We show that the effects of soil volume and plant density are largely interchangeable and that plants may use both SVS and RDS to detect their neighbours and to integrate growth responses to both volume and the presence of neighbours. Our work demonstrates the remarkable ability of plants to make proactive decisions about their growth, and has implications for mitigating the effects of dense sowing of crops in agricultural practice.

Plants use environmental cues to determine their optimal root and shoot growth. It is well known to gardeners and horticulturists alike that soil volume – most commonly in the form of pot size – strongly restricts plant growth, but the mechanisms by which this effect occurs remain unclear. Here, we show that shoot growth scales directly with soil volume, independently of the nutritional content of the soil, and that plants can become ‘volume restricted’ even in the presence of abundant resources. We show that plants can detect their soil volume as early as 3 weeks post germination, and that shoot growth restriction therefore constitutes a pro-active ‘decision’ by the plant to avoid resource limitation later in the life cycle. Shoot growth restriction is not directly linked to root growth restriction, and does not occur in response to the mechanical detection of the pot walls. Rather, we show that plants detect their soil volume by detecting the density of roots in the proximity of their root system. As such, volume restriction may be intimately connected with the mechanism by which plants sense and respond to the roots of other plants in the rhizosphere. Our work demonstrates the remarkable ability of plants to make pro-active decisions about their growth to ensure they can complete their cycle, and has important implications for agricultural practise regarding both nutrient use efficiency and yield.