There and back again: An evolutionary perspective on long-distance coordination of plant growth and development.

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.

A historical overview of long-distance signalling in plants.

Be it a small herb or a large tree, intra- and intercellular communication and long-distance signalling between distant organs are crucial for every aspect of plant development. The vascular system, comprising xylem and phloem, acts as a major conduit for the transmission of long-distance signals in plants. In addition to expanding our knowledge of vascular development, numerous reports in the past two decades revealed that selective populations of RNAs, proteins, and phytohormones function as mobile signals. Many of these signals were shown to regulate diverse physiological processes, such as flowering, leaf and root development, nutrient acquisition, crop yield, and biotic/abiotic stress responses. In this review, we summarize the significant discoveries made in the past 25 years, with emphasis on key mobile signalling molecules (mRNAs, proteins including RNA-binding proteins, and small RNAs) that have revolutionized our understanding of how plants integrate various intrinsic and external cues in orchestrating growth and development. Additionally, we provide detailed insights on the emerging molecular mechanisms that might control the selective trafficking and delivery of phloem-mobile RNAs to target tissues. We also highlight the cross-kingdom movement of mobile signals during plant-parasite relationships. Considering the dynamic functions of these signals, their implications in crop improvement are also discussed.

The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis.

The carnivorous sundew plant (Drosera capensis) captures prey using sticky tentacles. We investigated the tentacle and trap reactions in response to the electrical and jasmonate signalling evoked by different stimuli to reveal how carnivorous sundews recognize digestible captured prey in their traps. We measured the electrical signals, phytohormone concentration, enzyme activities and Chla fluorescence in response to mechanical stimulation, wounding or insect feeding in local and systemic traps. Seven new proteins in the digestive fluid were identified using mass spectrometry. Mechanical stimuli and live prey induced a fast, localized tentacle-bending reaction and enzyme secretion at the place of application. By contrast, repeated wounding induced a nonlocalized convulsive tentacle movement and enzyme secretion in local but also in distant systemic traps. These differences can be explained in terms of the electrical signal propagation and jasmonate accumulation, which also had a significant impact on the photosynthesis in the traps. The electrical signals generated in response to wounding could partially mimic a mechanical stimulation of struggling prey and might trigger a false alarm, confirming that the botanical carnivory and plant defence mechanisms are related. To trigger the full enzyme activity, the traps must detect chemical stimuli from the captured prey.

Distinct palisade tissue development processes promoted by leaf autonomous signalling and long-distance signalling in Arabidopsis thaliana.

Plants develop palisade tissue consisting of cylindrical mesophyll cells located at the adaxial side of leaves in response to high light. To understand high light signalling in palisade tissue development, we investigated leaf autonomous and long-distance signal responses of palisade tissue development using Arabidopsis thaliana. Illumination of a developing leaf with high light induced cell height elongation, whereas illumination of mature leaves with high light increased cell density and suppressed cell width expansion in palisade tissue of new leaves. Examination using phototropin1 phototropin2 showed that blue light signalling mediated by phototropins was involved in cell height elongation of the leaf autonomous response rather than the cell density increase induced by long-distance signalling. Hydrogen peroxide treatment induced cylindrical palisade tissue cell formation in both a leaf autonomous and long-distance manner, suggesting involvement of oxidative signals. Although constitutive expression of transcription factors involved in systemic-acquired acclimation to excess light, ZAT10 and ZAT12, induced cylindrical palisade tissue cell formation, knockout of these genes did not affect cylindrical palisade tissue cell formation. We conclude that two distinct signalling pathways - leaf autonomous signalling mostly dependent on blue light signalling and long-distance signalling from mature leaves that sense high light and oxidative stress - control palisade tissue development in A. thaliana.

Common and specific responses to availability of mineral nutrients and water.

Changes in resource (mineral nutrients and water) availability, due to their heterogeneous distribution in space and time, affect plant development. Plants need to sense these changes to optimize growth and biomass allocation by integrating root and shoot growth. Since a limited supply of water or nutrients can elicit similar physiological responses (the relative activation of root growth at the expense of shoot growth), similar underlying mechanisms may affect perception and acquisition of either nutrients or water. This review compares root and shoot responses to availability of different macronutrients and water. Attention is given to the roles of root-to-shoot signalling and shoot-to-root signalling, with regard to coordinating changes in root and shoot growth and development. Involvement of plant hormones in regulating physiological responses such as stomatal and hydraulic conductance is revealed by measuring the effects of resource availability on phytohormone concentrations in roots and shoots, and their flow between roots and shoots in xylem and phloem saps. More specific evidence can be obtained by measuring the physiological responses of genotypes with altered hormone responses or concentrations. We discuss the similarity and diversity of changes in shoot growth, allocation to root growth, and root architecture under changes in water, nitrate, and phosphorus availability, and the possible involvement of abscisic acid, indole-acetic acid, and cytokinin in their regulation. A better understanding of these mechanisms may contribute to better crop management for efficient use of these resources and to selecting crops for improved performance under suboptimal soil conditions.

FLOWERING LOCUS T has higher protein mobility than TWIN SISTER OF FT.

In plants, successful reproduction requires the proper timing of flowering under changing environmental conditions. Arabidopsis FLOWERING LOCUS T (FT), which encodes a proposed phloem-mobile florigen, has a close homologue, TWIN SISTER OF FT (TSF). During the vegetative phase, TSF shows high levels of expression in the hypocotyl before FT induction, but the tsf mutation does not have an apparent flowering-time phenotype on its own under long-day conditions. This study compared the protein mobility of FT and TSF. With TSF-overexpressing plants as the rootstock, the flowering time of ft tsf scion plants was only slightly accelerated. Previous work has shown that FT is graft-transmissible; by contrast, this study did not detect movement of TSF from the roots into the shoot of the scion plants. This study used plants overexpressing FT/TSF chimeric proteins to map a region responsible for FT movement. A chimeric TSF with region II of FT (L28 to G98) expressed in the rootstock caused early flowering in ft tsf scion plants; movement of the chimeric protein from the rootstocks into the shoot apical region of the ft tsf scion plants was also detected. Misexpression of TSF in the leaf under the control of the FT promoter or grafting of 35S::TSF cotyledons accelerated flowering of ft-10 plants. FT was more stable than TSF. Taking these results together, we propose that protein mobility of FT is higher than that of TSF, possibly due to a protein domain that confers mobility and/or protein stability.

The angiosperm phloem sieve tube system: a role in mediating traits important to modern agriculture.

The plant vascular system serves a vital function by distributing water, nutrients and hormones essential for growth and development to the various organs of the plant. In this review, attention is focused on the role played by the phloem as the conduit for delivery of both photosynthate and information macromolecules, especially from the context of its mediation in traits that are important to modern agriculture. Resource allocation of sugars and amino acids, by the phloem, to specific sink tissues is of importance to crop yield and global food security. Current findings are discussed in the context of a hierarchical control network that operates to integrate resource allocation to competing sinks. The role of plasmodesmata that connect companion cells to neighbouring sieve elements and phloem parenchyma cells is evaluated in terms of their function as valves, connecting the sieve tube pressure manifold system to the various plant tissues. Recent studies have also revealed that plasmodesmata and the phloem sieve tube system function cooperatively to mediate the long-distance delivery of proteins and a diverse array of RNA species. Delivery of these information macromolecules is discussed in terms of their roles in control over the vegetative-to-floral transition, tuberization in potato, stress-related signalling involving miRNAs, and genetic reprogramming through the delivery of 24-nucleotide small RNAs that function in transcriptional gene silencing in recipient sink organs. Finally, we discuss important future research areas that could contribute to developing agricultural crops with engineered performance characteristics for enhance yield potential.

Spread the news: systemic dissemination and local impact of Ca²âº signals along the phloem pathway.

We explored the idea of whether electropotential waves (EPWs) primarily act as vehicles for systemic spread of Ca(2+) signals. EPW-associated Ca(2+) influx may trigger generation and amplification of countless long-distance signals along the phloem pathway given the fact that gating of Ca(2+)-permeable channels is a universal response to biotic and abiotic challenges. Despite fundamental differences, both action and variation potentials are associated with a sudden Ca(2+) influx. Both EPWs probably disperse in the lateral direction, which could be of essential functional significance. A vast set of Ca(2+)-permeable channels, some of which have been localized, is required for Ca(2+)-modulated events in sieve elements. There, Ca(2+)-permeable channels are clustered and create so-called Ca(2+) hotspots, which play a pivotal role in sieve element occlusion. Occlusion mechanisms play a central part in the interaction between plants and phytopathogens (e.g. aphids or phytoplasmas) and in transient re-organization of the vascular symplasm. It is argued that Ca(2+)-triggered systemic signalling occurs in partly overlapping waves. The forefront of EPWs may be accompanied by a burst of free Ca(2+) ions and Ca(2+)-binding proteins in the sieve tube sap, with a far-reaching impact on target cells. Lateral dispersion of EPWs may induce diverse Ca(2+) influx and handling patterns (Ca(2+) signatures) in various cell types lining the sieve tubes. As a result, a variety of cascades may trigger the fabrication of signals such as phytohormones, proteins, or RNA species released into the sap stream after product-related lag times. Moreover, transient reorganization of the vascular symplasm could modify cascades in disjunct vascular cells.

Plasmodesmata-located protein overexpression negatively impacts the manifestation of systemic acquired resistance and the long-distance movement of Defective in Induced Resistance1 in Arabidopsis.

Systemic acquired resistance (SAR) is a plant defence response that provides immunity to distant uninfected leaves after an initial localised infection. The lipid transfer protein (LTP) Defective in Induced Resistance1 (DIR1) is an essential component of SAR that moves from induced to distant leaves following a SAR-inducing local infection. To understand how DIR1 is transported to distant leaves during SAR, we analysed DIR1 movement in transgenic Arabidopsis lines with reduced cell-to-cell movement caused by the overexpression of Plasmodesmata-Located Proteins PDLP1 and PDLP5. These PDLP-overexpressing lines were defective for SAR, and DIR1 antibody signals were not observed in phloem sap-enriched petiole exudates collected from distant leaves. Our data support the idea that cell-to-cell movement of DIR1 through plasmodesmata is important during long-distance SAR signalling in Arabidopsis.