In this study, the role of the recently identified class of phytohormones, strigolactones, in shaping root architecture was addressed. Primary root lengths of strigolactone-deficient and -insensitive Arabidopsis (Arabidopsis thaliana) plants were shorter than those of wild-type plants. This was accompanied by a reduction in meristem cell number, which could be rescued by application of the synthetic strigolactone analog GR24 in all genotypes except in the strigolactone-insensitive mutant. Upon GR24 treatment, cells in the transition zone showed a gradual increase in cell length, resulting in a vague transition point and an increase in transition zone size. PIN1/3/7-green fluorescent protein intensities in provascular tissue of the primary root tip were decreased, whereas PIN3-green fluorescent protein intensity in the columella was not affected. During phosphatesufficient conditions, GR24 application to the roots suppressed lateral root primordial development and lateral root forming potential, leading to a reduction in lateral root density. Moreover, auxin levels in leaf tissue were reduced. When auxin levels were increased by exogenous application of naphthylacetic acid, GR24 application had a stimulatory effect on lateral root development instead. Similarly, under phosphate-limiting conditions, endogenous strigolactones present in wild-type plants stimulated a more rapid outgrowth of lateral root primordia when compared with strigolactone-deficient mutants. These results suggest that strigolactones are able to modulate local auxin levels and that the net result of strigolactone action is dependent on the auxin status of the plant. We postulate that the tightly balanced auxin-strigolactone interaction is the basis for the mechanism of the regulation of the plants' root-to-shoot ratio.Strigolactones, exuded from plants, have been known for a long time to act as germination stimulants for seeds of root parasitic plants such as Orobanche and Striga spp. (for review, see Bouwmeester et al., 2003Bouwmeester et al., , 2007. As root parasitic plants consume a large proportion of the host plants' solutes, they cause wilting and early plant death. Initially, the discovery that strigolactones are also involved in the symbiotic interaction with arbuscular mycorrhizal fungi (Akiyama et al., 2005) was believed to provide an explanation for why the host plants' capacity to produce strigolactones was not lost during evolution. Because arbuscular mycorrhizal fungi are potent providers of nutrients such as phosphate (Pi) and nitrogen to their host, the observation that Pi starvation induced strigolactone biosynthesis in host plants' roots was not surprising (Yoneyama et al., 2007;Ló pez-Ráez et al., 2008). The recent discovery that strigolactones, or closely related compounds, also act as phytohormones inside the host plants and are involved in the inhibition of axillary bud outgrowth (Gomez-Roldan et al., 2008;Umehara et al., 2008) is an additional explanation why plants continue to produce these fatal ger-
Multicellular organisms activate immunity upon recognition of pathogen-associated molecular patterns (PAMPs). Chitin is the major component of fungal cell walls, and chitin oligosaccharides act as PAMPs in plant and mammalian cells. Microbial pathogens deliver effector proteins to suppress PAMP-triggered host immunity and to establish infection. Here, we show that the LysM domain-containing effector protein Ecp6 of the fungal plant pathogen Cladosporium fulvum mediates virulence through perturbation of chitin-triggered host immunity. During infection, Ecp6 sequesters chitin oligosaccharides that are released from the cell walls of invading hyphae to prevent elicitation of host immunity. This may represent a common strategy of host immune suppression by fungal pathogens, because LysM effectors are widely conserved in the fungal kingdom.
Strigolactones were originally identified as stimulators of the germination of root-parasitic weeds 1 that pose a serious threat to resource-limited agriculture 2 . They are mostly exuded from roots and function as signalling compounds in the initiation of arbuscular mycorrhizae 3 , which are plant-fungus symbionts with a global effect on carbon and phosphate cycling 4 . Recently, strigolactones were established to be phytohormones that regulate plant shoot architecture by inhibiting the outgrowth of axillary buds 5,6 . Despite their importance, it is not known how strigolactones are transported. ATP-binding cassette (ABC) transporters, however, are known to have functions in phytohormone translocation [7][8][9] . Here we show that the Petunia hybrida ABC transporter PDR1 has a key role in regulating the development of arbuscular mycorrhizae and axillary branches, by functioning as a cellular strigolactone exporter. P. hybrida pdr1 mutants are defective in strigolactone exudation from their roots, resulting in reduced symbiotic interactions. Above ground, pdr1 mutants have an enhanced branching phenotype, which is indicative of impaired strigolactone allocation. Overexpression of Petunia axillaris PDR1 in Arabidopsis thaliana results in increased tolerance to high concentrations of a synthetic strigolactone, consistent with increased export of strigolactones from the roots. PDR1 is the first known component in strigolactone transport, providing new opportunities for investigating and manipulating strigolactone-dependent processes.Strigolactones are a new class of carotenoid-derived 10 phytohormone in land plants. In addition to their role in shoot branching, strigolactones are exuded into the rhizosphere under phosphorus-limiting conditions 5 and act as growth stimulants of arbuscular mycorrhizal fungi 3 . To identify efflux carriers of arbuscular-mycorrhiza-promoting factors such as strigolactones, we used a degenerate primer approach ( Supplementary Fig. 2a) to isolate full-size PDR-type transporters (also known as ABC subtype G (ABCG) transporters) of P. hybrida that are abundant in phosphate-starved or mycorrhizal roots. The rationale behind the focus on these transporters, of which there are 15 in Arabidopsis 11 , 23 in Oryza sativa (rice) 11 and 23 putative factors in Solanum lycopersicum (tomato) ( Supplementary Fig. 3a), was that they are plasma membrane proteins often found in roots 12 , they are implicated in below-ground plantmicrobe interactions 13,14 , and they have affinities for compounds that are structurally related to strigolactones 8,9,15 . Of six primary candidates, only P. hybrida PDR1 had increased expression in roots that were subjected to either phosphate starvation (Fig. 1a) or colonization by the arbuscular mycorrhizal fungus Glomus intraradices (Fig. 1b). Furthermore, PDR1 transcript levels increased in response to treatment with the synthetic strigolactone analogue GR24 or the auxin analogue 1-naphthaleneacetic acid (NAA) (Fig. 1c). Auxin has been shown to upregulate strigolactone-bi...
The biosynthesis of the recently identified novel class of plant hormones, strigolactones, is up-regulated upon phosphate deficiency in many plant species. It is generally accepted that the evolutionary origin of strigolactone up-regulation is their function as a rhizosphere signal that stimulates hyphal branching of arbuscular mycorrhizal fungi. In this work, we demonstrate that this induction is conserved in Arabidopsis (Arabidopsis thaliana), although Arabidopsis is not a host for arbuscular mycorrhizal fungi. We demonstrate that the increase in strigolactone production contributes to the changes in shoot architecture observed in response to phosphate deficiency. Using high-performance liquid chromatography, column chromatography, and multiple reaction monitoring-liquid chromatography-tandem mass spectrometry analysis, we identified two strigolactones (orobanchol and orobanchyl acetate) in Arabidopsis and have evidence of the presence of a third (5-deoxystrigol). We show that at least one of them (orobanchol) is strongly reduced in the putative strigolactone biosynthetic mutants more axillary growth1 (max1) and max4 but not in the signal transduction mutant max2. Orobanchol was also detected in xylem sap and up-regulated under phosphate deficiency, which is consistent with the idea that root-derived strigolactones are transported to the shoot, where they regulate branching. Moreover, two additional putative strigolactone-like compounds were detected in xylem sap, one of which was not detected in root exudates. Together, these results show that xylem-transported strigolactones contribute to the regulation of shoot architectural response to phosphate-limiting conditions.
ORCID IDs: 0000-0002-9014-9516 (D.V.); 0000-0001-8918-0711 (J.J.B.K.).Quantitative traits in plants are controlled by a large number of genes and their interaction with the environment. To disentangle the genetic architecture of such traits, natural variation within species can be explored by studying genotype-phenotype relationships. Genome-wide association studies that link phenotypes to thousands of single nucleotide polymorphism markers are nowadays common practice for such analyses. In many cases, however, the identified individual loci cannot fully explain the heritability estimates, suggesting missing heritability. We analyzed 349 Arabidopsis accessions and found extensive variation and high heritabilities for different morphological traits. The number of significant genome-wide associations was, however, very low. The application of genomic prediction models that take into account the effects of all individual loci may greatly enhance the elucidation of the genetic architecture of quantitative traits in plants. Here, genomic prediction models revealed different genetic architectures for the morphological traits. Integrating genomic prediction and association mapping enabled the assignment of many plausible candidate genes explaining the observed variation. These genes were analyzed for functional and sequence diversity, and good indications that natural allelic variation in many of these genes contributes to phenotypic variation were obtained. For ACS11, an ethylene biosynthesis gene, haplotype differences explaining variation in the ratio of petiole and leaf length could be identified.The natural phenomena of mutation and recombination that change the genetic code with each generation have given rise to the enormous genetic diversity between and within species. Through evolutionary processes, such as drift, migration, and selection, plants have accumulated a vast number of molecular polymorphisms that enabled adaptation to a wide range of environments (Kooke and Keurentjes, 2012). With the recent advancements in genetic and genomic tools, this nucleotide diversity can be fully surveyed to identify causal polymorphisms for many different plant phenotypes. This should allow the identification of molecular changes that provided evolutionary advantages and beneficial characteristics in agronomically important traits.Through selection on variation in performance, plants have adapted to different environments. Plant performance is directly determined by life history traits, such as flowering time and growth rate, which in turn depend on genetics, morphology, physiology, and the environment (Roff, 2007;Kooke et al., 2015). Understanding the regulation of plant growth and morphology is therefore essential for the comprehension of plant performance. Arabidopsis has adapted to a wide range of environments and displays an extensive variety in morphological and growth-related phenotypes. Its small genome size, the publicly available
In the natural environment, days are generally warmer than the night, resulting in a positive day/night temperature difference (+DIF). Plants have adapted to these conditions, and when exposed to antiphase light and temperature cycles (cold photoperiod/ warm night [2DIF]), most species exhibit reduced elongation growth. To study the physiological mechanism of how light and temperature cycles affect plant growth, we used infrared imaging to dissect growth dynamics under +DIF and 2DIF in the model plant Arabidopsis (Arabidopsis thaliana). We found that 2DIF altered leaf growth patterns, decreasing the amplitude and delaying the phase of leaf movement. Ethylene application restored leaf growth in 2DIF conditions, and constitutive ethylene signaling mutants maintain robust leaf movement amplitudes under 2DIF, indicating that ethylene signaling becomes limiting under these conditions. In response to 2DIF, the phase of ethylene emission advanced 2 h, but total ethylene emission was not reduced. However, expression analysis on members of the 1-aminocyclopropane-1-carboxylic acid (ACC) synthase ethylene biosynthesis gene family showed that ACS2 activity is specifically suppressed in the petiole region under 2DIF conditions. Indeed, petioles of plants under 2DIF had reduced ACC content, and application of ACC to the petiole restored leaf growth patterns. Moreover, acs2 mutants displayed reduced leaf movement under +DIF, similar to wild-type plants under 2DIF. In addition, we demonstrate that the photoreceptor PHYTOCHROME B restricts ethylene biosynthesis and constrains the 2DIF-induced phase shift in rhythmic growth. Our findings provide a mechanistic insight into how fluctuating temperature cycles regulate plant growth.
We show that antiphase light-temperature cycles (negative day-night temperature difference [2DIF]) inhibit hypocotyl growth in Arabidopsis (Arabidopsis thaliana). This is caused by reduced cell elongation during the cold photoperiod. Cell elongation in the basal part of the hypocotyl under 2DIF was restored by both 1-aminocyclopropane-1-carboxylic acid (ACC; ethylene precursor) and auxin, indicating limited auxin and ethylene signaling under 2DIF. Both auxin biosynthesis and auxin signaling were reduced during 2DIF. In addition, expression of several ACC Synthase was reduced under 2DIF but could be restored by auxin application. In contrast, the reduced hypocotyl elongation of ethylene biosynthesis and signaling mutants could not be complemented by auxin, indicating that auxin functions upstream of ethylene. The PHYTOCHROME INTERACTING FACTORS (PIFs) PIF3, PIF4, and PIF5 were previously shown to be important regulators of hypocotyl elongation. We now show that, in contrast to pif4 and pif5 mutants, the reduced hypocotyl length in pif3 cannot be rescued by either ACC or auxin. In line with this, treatment with ethylene or auxin inhibitors reduced hypocotyl elongation in PIF4 overexpressor (PIF4ox) and PIF5ox but not PIF3ox plants. PIF3 promoter activity was strongly reduced under 2DIF but could be restored by auxin application in an ACC Synthase-dependent manner. Combined, these results show that PIF3 regulates hypocotyl length downstream, whereas PIF4 and PIF5 regulate hypocotyl length upstream of an auxin and ethylene cascade. We show that, under 2DIF, lower auxin biosynthesis activity limits the signaling in this pathway, resulting in low activity of PIF3 and short hypocotyls.
BackgroundQuantification of leaf movement is an important tool for characterising the effects of environmental signals and the circadian clock on plant development. Analysis of leaf movement is currently restricted by the attachment of sensors to the plant or dependent upon visible light for time-lapse photography. The study of leaf growth movement rhythms in mature plants under biological relevant conditions, e.g. diurnal light and dark conditions, is therefore problematic.ResultsHere we present OSCILLATOR, an affordable system for the analysis of rhythmic leaf growth movement in mature plants. The system contains three modules: (1) Infrared time-lapse imaging of growing mature plants (2) measurement of projected distances between leaf tip and plant apex (leaf tip tracking growth-curves) and (3) extraction of phase, period and amplitude of leaf growth oscillations using wavelet analysis. A proof-of-principle is provided by characterising parameters of rhythmic leaf growth movement of different Arabidopsis thaliana accessions as well as of Petunia hybrida and Solanum lycopersicum plants under diurnal conditions. The amplitude of leaf oscillations correlated to published data on leaf angles, while amplitude and leaf length did not correlate, suggesting a distinct leaf growth profile for each accession. Arabidopsis mutant accession Landsberg erecta displayed a late phase (timing of peak oscillation) compared to other accessions and this trait appears unrelated to the ERECTA locus.ConclusionsOSCILLATOR is a low cost and easy to implement system that can accurately and reproducibly quantify rhythmic growth of mature plants for different species under diurnal light/dark cycling.
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