Michael Riemann

Impaired Induction of the Jasmonate Pathway in the Rice Mutant hebiba

The elongation of rice (Oryza sativa) coleoptiles is inhibited by light, and this photoinhibition was used to screen for mutants with impaired light response. In one of the isolated mutants, hebiba, coleoptile elongation was stimulated in the presence of red light, but inhibited in the dark. Light responses of endogenous indolyl-3-acetic acid and abscisic acid were identical between the wild type and the mutant. In contrast, the wild type showed a dramatic increase of jasmonate heralded by corresponding increases in the content of its precursor o-phytodienoic acid, whereas both compounds were not detectable in the mutant. The jasmonate response to wounding was also blocked in the mutant. The mutant phenotype was rescued by addition of exogenous methyl jasmonate and o-phytodienoic acid. Moreover, the expression of O. sativa 12-oxophytodienoic acid reductase, an early gene of jasmonic acid-synthesis, is induced by red light in the wild type, but not in the mutant. This evidence suggests a novel role for jasmonates in the light response of growth, and we discuss a cross-talk between jasmonate and auxin signaling. In addition, hebiba represents the first rice mutant in which the induction of the jasmonate pathway is impaired providing a valuable tool to study the role of jasmonates in Graminean development.

The host guides morphogenesis and stomatal targeting in the grapevine pathogen Plasmopara viticola.

Abstract. The oomycete grape downy mildew (Plasmopara viticola Berk. & Curt. Ex de Bary) is a serious pathogen of grapevine and spreads by extremely efficient cycles of asexual propagation. The high efficiency must involve efficient sensing of the host. We therefore analyzed the time course and morphology of the early development of this pathogen in a host system, by infection of leaf discs of grapevine (Vitis vinifera L. cv. Müller-Thurgau), and in a host-free system. Host factors were demonstrated to influence pathogen development in the following ways: (i) the release of zoospores from mature sporangia was accelerated, (ii) the morphogenesis of the germ tube was coordinated, and (iii) the zoospores were targeted to the stomata by factors that depended on stomata closure. The findings show that the early development of P. viticola is regulated, specifically and coordinately, by factors originating from the host plant.

The jasmonate pathway mediates salt tolerance in grapevines

Salt stress is a major constraint for many crop plants, such as the moderately salt-sensitive economically important fruit crop grapevine. Plants have evolved different strategies for protection against salinity and drought. Jasmonate signalling is a central element of both biotic and abiotic stress responses. To discriminate stress quality, there must be cross-talk with parallel signal chains. Using two grapevine cell lines differing in salt tolerance, the response of jasmonate ZIM/tify-domain (JAZ/TIFY) proteins (negative regulators of jasmonate signalling), a marker for salt adaptation Na+/H+ EXCHANGER (NHX1), and markers for biotic defence STILBENE SYNTHASE (StSy) and RESVERATROL SYNTHASE (RS) were analysed. It is shown that salt stress signalling shares several events with biotic defence including activity of a gadolinium-sensitive calcium influx channel (monitored by apoplastic alkalinization) and transient induction of JAZ/TIFY transcripts. Exogenous jasmonate can rescue growth in the salt-sensitive cell line. Suppression of jasmonate signalling by phenidone or aspirin blocks the induction of JAZ/TIFY transcripts. The rapid induction of RS and StSy characteristic for biotic defence in grapevine is strongly delayed in response to salt stress. In the salt-tolerant line, NHX1 is induced and the formation of reactive oxygen species, monitored as stress markers in the sensitive cell line, is suppressed. The data are discussed in terms of a model where salt stress signalling acts as a default pathway whose readout is modulated by a parallel signal chain triggered by biotic factors downstream of jasmonate signalling.

Rice JASMONATE RESISTANT 1 is involved in phytochrome and jasmonate signalling

Jasmonic acid (JA) is an important negative regulator of light-regulated coleoptile elongation in rice. We isolated rice JASMONATE RESISTANT 1 (osjar1) mutants from the Tos17 mutant panel by BLAST search. In far-red and blue lights, osjar1 coleoptiles were longer if compared with the wild type (WT), indicating that OsJar1 participates in the suppression of coleoptile elongation in these light conditions, while the mutant did not show a clear phenotype in red light. The analysis of OsJar1 expression in phytochrome (phy) mutants revealed that phytochrome A (phyA) and phytochrome B (phyB) act redundantly to induce this gene by red light, presumably. Unexpectedly, blue light-induced expression of OsJar1 gene was impaired in phyA-deficient mutants, indicating the involvement of phyA in the blue light signalling. In WT seedlings, OsJar1 transcripts were up-regulated transiently in response to treatment with exogenous methyl-jasmonic acid (MeJA). The dose-response curve of the MeJA treatment showed a characteristic pattern: concentrations as low as 4.5 nM could induce OsJar1 transcription, while the gene was superinduced at a concentration of 450 microM MeJA. In summary, this paper demonstrated that OsJar1 modulates light and JA signalling in the photomorphogenesis of rice.

Exploring Jasmonates in the Hormonal Network of Drought and Salinity Responses

Present and future food security is a critical issue compounded by the consequences of climate change on agriculture. Stress perception and signal transduction in plants causes changes in gene or protein expression which lead to metabolic and physiological responses. Phytohormones play a central role in the integration of different upstream signals into different adaptive outputs such as changes in the activity of ion-channels, protein modifications, protein degradation, and gene expression. Phytohormone biosynthesis and signaling, and recently also phytohormone crosstalk have been investigated intensively, but the function of jasmonates under abiotic stress is still only partially understood. Although most aspects of jasmonate biosynthesis, crosstalk and signal transduction appear to be similar for biotic and abiotic stress, novel aspects have emerged that seem to be unique for the abiotic stress response. Here, we review the knowledge on the role of jasmonates under drought and salinity. The crosstalk of jasmonate biosynthesis and signal transduction pathways with those of abscisic acid (ABA) is particularly taken into account due to the well-established, central role of ABA under abiotic stress. Likewise, the accumulating evidence of crosstalk of jasmonate signaling with other phytohormones is considered as important element of an integrated phytohormonal response. Finally, protein post-translational modification, which can also occur without de novo transcription, is treated with respect to its implications for phytohormone biosynthesis, signaling and crosstalk. To breed climate-resilient crop varieties, integrated understanding of the molecular processes is required to modulate and tailor particular nodes of the network to positively affect stress tolerance.

Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex

Early stages of a beneficial relationship Plants benefit from widespread symbiosis with arbuscular mycorrhizal fungi. This symbiosis between plant and fungus aids plants in capturing mineral and micronutrients from the soil. Gutjahr et al. have now identified a component of an intracellular receptor, the hydrolase DWARF 14 LIKE, required in rice roots for initiating the symbiosis. A similar receptor detects karrikins in smoke that signal opportunity for fireweed to grow after a forest fire. Science, this issue p. 1521 Widely beneficial symbiosis between plant and fungi shares signaling components with wildfire ephemerals. In terrestrial ecosystems, plants take up phosphate predominantly via association with arbuscular mycorrhizal fungi (AMF). We identified loss of responsiveness to AMF in the rice (Oryza sativa) mutant hebiba, reflected by the absence of physical contact and of characteristic transcriptional responses to fungal signals. Among the 26 genes deleted in hebiba, DWARF 14 LIKE is, the one responsible for loss of symbiosis . It encodes an alpha/beta-fold hydrolase, that is a component of an intracellular receptor complex involved in the detection of the smoke compound karrikin. Our finding reveals an unexpected plant recognition strategy for AMF and a previously unknown signaling link between symbiosis and plant development.

RSOsPR10 Expression in Response to Environmental Stresses is Regulated Antagonistically by Jasmonate/Ethylene and Salicylic Acid Signaling Pathways in Rice Roots

Plant roots play important roles not only in the absorption of water and nutrients, but also in stress tolerance. Previously, we identified RSOsPR10 as a root-specific pathogenesis-related (PR) protein induced by drought and salt treatments in rice. Transcripts and proteins of RSOsPR10 were strongly induced by jasmonate (JA) and the ethylene (ET) precursor 1-aminocyclopropane-1-carboxylic acid (ACC), while salicylic acid (SA) almost completely suppressed these inductions. Immunohistochemical analyses showed that RSOsPR10 strongly accumulated in cortex cells surrounding the vascular system of roots, and this accumulation was also suppressed when SA was applied simultaneously with stress or hormone treatments. In the JA-deficient mutant hebiba, RSOsPR10 expression was up-regulated by NaCl, wounding, drought and exogenous application of JA. This suggested the involvement of a signal transduction pathway that integrates JA and ET signals in plant defense responses. Expression of OsERF1, a transcription factor in the JA/ET pathway, was induced earlier than that of RSOsPR10 after salt, JA and ACC treatments. Simultaneous SA treatment strongly inhibited the induction of RSOsPR10 expression and, to a lesser extent, induction of OsERF1 expression. These results suggest that JA/ET and SA pathways function in the stress-responsive induction of RSOsPR10, and that OsERF1 may be one of the transcriptional factors in the JA/ET pathway.

A role for actin-driven secretion in auxin-induced growth

Summary. In epidermal cells of Zea mays coleoptiles, actin microfilaments are organized in fine strands during cell elongation, but are bundled in response to signals that inhibit growth. This bundling response is accompanied by an increased membrane association of extracted actin. Brefeldin A, an inhibitor of vesicle secretion, increases the membrane association of actin, causes a bundling of cortical actin microfilaments, and reduces the sensitivity of cell elongation to auxin. A model is proposed where auxin controls the dynamics of an actin subpopulation that guides vesicles loaded with components of the auxin-signaling machinery towards the cell poles.

Cholodny-Went revisited: a role for jasmonate in gravitropism of rice coleoptiles

Gravitropism is explained by the Cholodny–Went hypothesis: the basipetal flow of auxin is diverted laterally. The resulting lateral auxin gradient triggers asymmetric growth. However, the Cholodny–Went hypothesis has been questioned repeatedly because the internal auxin gradient is too small to account for the observed growth asymmetry. Therefore, an additional gradient in indolyl-3-acetic acid (IAA) sensitivity has been suggested (Brauner and Hager in Planta 51:115–147, 1958). We challenged the Cholodny–Went hypothesis for gravitropism of rice coleoptiles (Oryza sativa L.) and found it to be essentially true. However, we observed, additionally, that the two halves of gravitropically stimulated coleoptiles responded differentially to the same amount of exogenous auxin: the auxin response is reduced in the upper flank but normal in the lower flank. This indicates that the auxin-gradient is amplified by a gradient of auxin responsiveness. Hormone contents were measured across the coleoptile by a GC-MS/MS technique and a gradient of jasmonate was detected opposing the auxin gradient. Furthermore, the total content of jasmonate increased during the gravitropic response. Jasmonate gradient and increase persist even when the lateral IAA gradient is inhibited by 1-N-naphtylphtalamic acid. Flooding with jasmonate delays the onset of gravitropic bending. Moreover, a jasmonate-deficient rice mutant bends more slowly and later than the wild type. We discuss a role of jasmonate as modulator of auxin responsiveness in gravitropism.

Induced Jasmonate Signaling Leads to Contrasting Effects on Root Damage and Herbivore Performance

Jasmonates reduce root damage by belowground herbivores, but enhanced jasmonate biosynthesis improves herbivore growth. Induced defenses play a key role in plant resistance against leaf feeders. However, very little is known about the signals that are involved in defending plants against root feeders and how they are influenced by abiotic factors. We investigated these aspects for the interaction between rice (Oryza sativa) and two root-feeding insects: the generalist cucumber beetle (Diabrotica balteata) and the more specialized rice water weevil (Lissorhoptrus oryzophilus). Rice plants responded to root attack by increasing the production of jasmonic acid (JA) and abscisic acid, whereas in contrast to in herbivore-attacked leaves, salicylic acid and ethylene levels remained unchanged. The JA response was decoupled from flooding and remained constant over different soil moisture levels. Exogenous application of methyl JA to the roots markedly decreased the performance of both root herbivores, whereas abscisic acid and the ethylene precursor 1-aminocyclopropane-1-carboxylic acid did not have any effect. JA-deficient antisense 13-lipoxygenase (asLOX) and mutant allene oxide cyclase hebiba plants lost more root biomass under attack from both root herbivores. Surprisingly, herbivore weight gain was decreased markedly in asLOX but not hebiba mutant plants, despite the higher root biomass removal. This effect was correlated with a herbivore-induced reduction of sucrose pools in asLOX roots. Taken together, our experiments show that jasmonates are induced signals that protect rice roots from herbivores under varying abiotic conditions and that boosting jasmonate responses can strongly enhance rice resistance against root pests. Furthermore, we show that a rice 13-lipoxygenase regulates root primary metabolites and specifically improves root herbivore growth.