Local HY5 Activity Mediates Hypocotyl Growth and Shoot-to-Root Communication

Burko, Yogev; Gaillochet, Christophe; Seluzicki, Adam; Chory, Joanne; Busch, Wolfgang

doi:10.1016/j.xplc.2020.100078

Cited by 37 publications

(31 citation statements)

References 44 publications

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“…Notably, the direct application of FR light to roots did not reduce LR density, indicating that shoot-derived HY5 protein may play a role in lateral root inhibition [50]. In line with this, HY5 expression driven by the HY5 native or phloem companion cell-specific SUCROSE-PROTON SYMPORTER 2 (SUC2) promoter suppressed lateral root growth in shade, which supports the idea that HY5 acts via the phloem [51]. More recent results have questioned the necessity of HY5 translocation in its regulation of root elongation [51].…”

Section: Top-down Organization: Shoot To Root Signalssupporting

confidence: 64%

“…In line with this, HY5 expression driven by the HY5 native or phloem companion cell-specific SUCROSE-PROTON SYMPORTER 2 (SUC2) promoter suppressed lateral root growth in shade, which supports the idea that HY5 acts via the phloem [51]. More recent results have questioned the necessity of HY5 translocation in its regulation of root elongation [51]. HY5 fused to an N-terminal hemagglutinin (HA)-YFP-HA ('DOF') tag expressed in the shoots was undetectable in roots, but still rescued the short root phenotype of the hy5 mutant.…”

Section: Top-down Organization: Shoot To Root Signalssupporting

confidence: 63%

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How roots and shoots communicate through stressful times

Testerink

Zhang

2021

Trends in Plant Science

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When plants face an environmental stress such as water deficit, soil salinity, high temperature, or shade, good communication between above-and belowground organs is necessary to coordinate growth and development. Various signals including hormones, peptides, proteins, hydraulic signals, and metabolites are transported mostly through the vasculature to distant tissues. How shoots and roots synchronize their response to stress using mobile signals is an emerging field of research. We summarize recent advances on mobile signals regulating shoot stomatal movement and root development in response to highly localized environmental cues. In addition, we highlight how the vascular system is not only a conduit but is also flexible in its development in response to abiotic stress. Shoot-root communication: a long-distance relationship Tissues in higher plants are highly specialized. The shoot captures solar energy by photosynthesis and carries out reproduction, whereas the root extracts water and minerals from the soil. The coordination of these specialized functions is critical for plants to thrive. The plant vascular system, comprising xylem and phloem (see Glossary), supports the plant body while also transporting many signaling molecules from shoots to roots and vice versa. Hormones are well-studied integrators of root and shoot development. Abscisic acid (ABA) [1], auxin [2], gibberellins [3], cytokinins (CKs) [4], and jasmonic acid and its relatives [5] are known to travel through the vasculature and to act in distant tissues (Figure 1, Key figure). More recently, several small peptides, proteins, and RNA molecules have been found to be mobile in xylem or phloem and to coordinate nutrient uptake and distal stress responses [6-10] (Figure 1).Localized environmental stresses such as soil salinity or light signals require controlled longdistance transport of stress signals to elicit acclimation responses at the whole-plant level [11,12]. Understanding how mobile signals activate distal stress-responsive signaling pathways and how local and distant developmental pathways are reprogrammed is an important aspect of abiotic stress tolerance. The long-distance signaling that mediates the nutrient stress response has been recently reviewed [7]. In this review we focus on recent developments in how different mobile signals coordinate shoot stomatal movements and root development in response to salinity, water-related stresses, and light and temperature changes. Furthermore, we highlight the developmental plasticity of the plant vascular system which is the central transportation path that allows mobile signals to travel over long distances in times of stress. Bottom-up approaches: stressed roots signal to shootsRoot-derived hydraulic signals mediate the plant shoot stress response Water limitation has a profound impact on plant growth [13]. Water absorbed from the soil moves radially to the root xylem both via the apoplastic pathway and via cell-to-cell pathways through transcellular transport and the symplastic pathway. Subs...

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Section: Top-down Organization: Shoot To Root Signalssupporting

confidence: 64%

Section: Top-down Organization: Shoot To Root Signalssupporting

confidence: 63%

How roots and shoots communicate through stressful times

Testerink

Zhang

2021

Trends in Plant Science

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“…Additionally, flavonoid precursors can be transported both short and long distances ( 64 , 65 ), which could allow a role for flavonols in long distance signaling. Several recent studies have illustrated important roles of long-distance root to shoot signal transport in controlling root development ( 88 ). The HY5 transcription factor named for its control of hypocotyl elongation also regulates primary root elongation and lateral root emergence, via mediating interactions between light and auxin signaling.…”

Section: Discussionmentioning

confidence: 99%

“…Light-dependent synthesis of flavonols is positively regulated by this transcription factor ( 89 ). HY5 was suggested to move as a long-distance signal from the shoot to the root, but recent findings suggest HY5 controls synthesis of this mobile signal ( 88 ). An intriguing possibility is that HY5-regulated flavonoid precursors produced in the shoot tissue may act as a long-distance signal leading to altered root architecture due to shoot-mediated environmental signals.…”

Section: Discussionmentioning

confidence: 99%

Flavonols modulate lateral root emergence by scavenging reactive oxygen species in Arabidopsis thaliana

Chapman

Muday

2021

Journal of Biological Chemistry

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Flavonoids are a class of specialized metabolites with subclasses including flavonols and anthocyanins, which have unique properties as antioxidants. Flavonoids modulate plant development, but whether and how they impact lateral root development is unclear. We examined potential roles for flavonols in this process using Arabidopsis thaliana mutants with defects in genes encoding key enzymes in flavonoid biosynthesis. We observed the tt4 and fls1 mutants, which produce no flavonols, have increased lateral root emergence. The tt4 root phenotype was reversed by genetic and chemical complementation. To more specifically define the flavonoids involved, we tested an array of flavonoid biosynthetic mutants, eliminating roles for anthocyanins and the flavonols quercetin and isorhamnetin in modulating lateral root development. Instead, two tt7 mutant alleles, with defects in a branchpoint enzyme blocking quercetin biosynthesis, formed reduced numbers of lateral roots and tt7-2 had elevated levels of kaempferol. Using a flavonol-specific dye, we observed that in the tt7-2 mutant, kaempferol accumulated within lateral root primordia at higher levels than wild-type. These data are consistent with kaempferol, or downstream derivatives, acting as a negative regulator of lateral root emergence. We examined ROS accumulation using ROS-responsive probes and found reduced fluorescence of a superoxide-selective probe within the primordia of tt7-2 compared with wild-type, but not in the tt4 mutant, consistent with opposite effects of these mutants on lateral root emergence. These results support a model in which increased level of kaempferol in the lateral root primordia of tt7 -2 reduces superoxide concentration and ROS-stimulated lateral root emergence.

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“…Additionally, flavonoid precursors can be transported both short and long distances (58,59), which could implicate a role for flavonols in long distance signaling. Several recent studies have illustrated important roles of long-distance root to shoot signal transport in controlling root development (79). The HY5 transcription factor named for its control of hypocotyl elongation, also regulates primary root elongation and lateral root emergence, via mediating interactions between light and auxin signaling.…”

Section: Discussionmentioning

confidence: 99%

Flavonols modulate lateral root emergence by scavenging reactive oxygen species inArabidopsis thaliana

Chapman

Muday

2020

Preprint

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Flavonoids are plant-specific antioxidant compounds that modulate plant development, which include flavonols and anthocyanins subclasses. In Arabidopsis thaliana, mutants in genes encoding each step in the flavonoid biosynthetic pathway have been isolated. We used these mutants to examine the role of flavonols in initiation and emergence of lateral roots and asked whether this regulation occurs through scavenging ROS. The tt4 mutants have a defect in the first committed step of flavonoid biosynthesis and have increased lateral root emergence. This phenotype was reversed by both genetic and chemical complementation. Using these flavonoid biosynthetic mutants, we eliminated roles for anthocyanins and the flavonols, quercetin and isorhamnetin, in controlling lateral root development. The tt7-2 mutant has a defect in a branchpoint enzyme blocking quercetin biosynthesis that led to elevated levels of kaempferol and reduced lateral roots. Kaempferol accumulated within lateral root primordia and was significantly increased in tt7-2. Thee data are consistent with kaempferol acting as a negative regulator of lateral root emergence. We examined ROS accumulation above and within the primordia using a general ROS sensor and identified increased signal above the primordia of the tt4 and tt7-2 mutants compared to wild type. Using a superoxide specific sensor, we detected a decrease in signal within the primordia of tt7-2, but not the tt4 mutant, compared to wild type. Together, these results support a model in which increased level of kaempferol in tt7-2 leads to a reduction in superoxide concentration in the lateral root primordia thereby reducing ROS-stimulated lateral root emergence.

show abstract

Local HY5 Activity Mediates Hypocotyl Growth and Shoot-to-Root Communication

Cited by 37 publications

References 44 publications

How roots and shoots communicate through stressful times

How roots and shoots communicate through stressful times

Flavonols modulate lateral root emergence by scavenging reactive oxygen species in Arabidopsis thaliana

Flavonols modulate lateral root emergence by scavenging reactive oxygen species inArabidopsis thaliana

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