AtBBX29 integrates photomorphogenesis and defense responses in Arabidopsis.

Light is an environmental signal that modulates plant defenses against attackers. Recent research has focused on the effects of light on defense hormone signaling; however, the connections between light signaling pathways and the biosynthesis of specialized metabolites involved in plant defense have been relatively unexplored. Here, we show that Arabidopsis BBX29, a protein that belongs to the B-Box transcription factor (TF) family, integrates photomorphogenic signaling with defense responses by promoting flavonoid, sinapate and glucosinolate accumulation in Arabidopsis leaves. AtBBX29 transcript levels were up regulated by light, through photoreceptor signaling pathways. Genetic evidence indicated that AtBBX29 up-regulates MYB12 gene expression, a TF known to induce genes related to flavonoid biosynthesis in a light-dependent manner, and MYB34 and MYB51, which encode TFs involved in the regulation of glucosinolate biosynthesis. Thus, bbx29 knockout mutants displayed low expression levels of key genes of the flavonoid biosynthetic pathway, and the opposite was true in BBX29 overexpression lines. In agreement with the transcriptomic data, bbx29 mutant plants accumulated lower levels of kaempferol glucosides, sinapoyl malate, indol-3-ylmethyl glucosinolate (I3M), 4-methylsulfinylbutyl glucosinolate (4MSOB) and 3-methylthiopropyl glucosinolate (3MSP) in rosette leaves compared to the wild-type, and showed increased susceptibility to the necrotrophic fungus Botrytis cinerea and to the herbivore Spodoptera frugiperda. In contrast, BBX29 overexpressing plants displayed increased resistance to both attackers. In addition, we found that AtBBX29 plays an important role in mediating the effects of ultraviolet-B (UV-B) radiation on plant defense against B. cinerea. Taken together, these results suggest that AtBBX29 orchestrates the accumulation of specific light-induced metabolites and regulates Arabidopsis resistance against pathogens and herbivores.

Ontogenetic and trans-generational dynamics of a vertically transmitted fungal symbiont in an annual host plant in ozone-polluted settings.

Tropospheric ozone is an abiotic stress of increasing importance in the context of global climate change. This greenhouse gas is a potent phytotoxic molecule with demonstrated negative effects on crop yield and natural ecosystems. Recently, oxidative stress has been proposed as a mechanism that could regulate the interaction between cool-season grasses and Epichloë endophytes. We hypothesized that exposure of Lolium multiflorum plants, hosting endophytes to an ozone-polluted environment at different ontogenetic phases, would impact the trans-generational dynamics of the vertically transmitted fungal symbiont. Here, we found that the ozone-induced stress on the mother plants did not affect the endophyte vertical transmission but it impaired the persistence of the fungus in the seed exposed to artificial ageing. Endophyte longevity in seed was reduced by exposure of the mother plant to ozone. Although ozone exposure did not influence either the endophyte mycelial concentration or their compound defences (loline alkaloids), a positive correlation was observed between host fitness and the concentration of endophyte-derived defence compounds. This suggests that fungal defences in grass seeds were not all produced in situ but remobilized from the vegetative tissues. Our study reveals ozone trans-generational effects on the persistence of a beneficial symbiont in a host grass.

Exploring growth-defence trade-offs in Arabidopsis: phytochrome B inactivation requires JAZ10 to suppress plant immunity but not to trigger shade-avoidance responses.

Under conditions that involve a high risk of competition for light among neighbouring plants, shade-intolerant species often display increased shoot elongation and greater susceptibility to pathogens and herbivores. The functional links between morphological and defence responses to crowding are not well understood. In Arabidopsis, the protein JAZ10 is thought to play a key role connecting the inactivation of the photoreceptor phytochrome B (phyB), which takes place under competition for light, with the repression of jasmonate-mediated plant defences. Here, we show that a null mutation of the JAZ10 gene in Arabidopsis did not affect plant growth nor did it suppress the shade-avoidance responses elicited by phyB inactivation. However, the jaz10 mutation restored many of the defence traits that are missing in the phyB mutant, including the ability to express robust responses to jasmonate and to accumulate indolic glucosinolates. Furthermore, the jaz10phyB double mutant showed a significantly increased resistance to the pathogenic fungus Botrytis cinerea compared with the phyB parental line. Our results demonstrate that, by inactivating JAZ10, it is possible to partially uncouple shade avoidance from defence suppression in Arabidopsis. These findings may provide clues to improve plant resistance to pathogens in crops that are planted at high density.

Linking phytochrome to plant immunity: low red : far-red ratios increase Arabidopsis susceptibility to Botrytis cinerea by reducing the biosynthesis of indolic glucosinolates and camalexin.

Shade-intolerant plants respond to low red : far-red (R : FR) ratios, which signal the proximity of potential competitors, by down-regulating immune responses. Here we investigated the mechanisms underlying this immune suppression in Arabidopsis. We used genetic, transcriptomic and metabolomic approaches to examine the functional connections between R : FR ratio and Arabidopsis resistance to the fungus Botrytis cinerea. Low R : FR ratios reduced the concentration of indol-3-ylmethyl glucosinolate (I3M) (an indolic glucosinolate, iGS) and camalexin in plants inoculated with B. cinerea, and attenuated the I3M response triggered by jasmonate elicitation. These effects on metabolite abundance correlated with reduced expression of iGS and camalexin biosynthetic genes. Furthermore, the effect of low R : FR increasing Arabidopsis susceptibility to B. cinerea was not present in mutants deficient in the biosynthesis of camalexin (pad3) or metabolism of iGS (pen2). Finally, in a mutant deficient in the JASMONATE ZIM DOMAIN-10 (JAZ10) protein, which does not respond to low R : FR with increased susceptibility to B. cinerea, supplemental FR failed to down-regulate iGS production. These results indicate that suppression of Arabidopsis immunity against B. cinerea by low R : FR ratios is mediated by reduced levels of Trp-derived defenses, and provide further evidence for a functional role of JAZ10 in the link between phytochrome and jasmonate signaling.

Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism.

Light is an important modulator of plant immune responses. Here, we show that inactivation of the photoreceptor phytochrome B (phyB) by a low red/far-red ratio (R:FR), which is a signal of competition in plant canopies, down-regulates the expression of defense markers induced by the necrotrophic fungus Botrytis cinerea, including the genes that encode the transcription factor ETHYLENE RESPONSE FACTOR1 (ERF1) and the plant defensin PLANT DEFENSIN1.2 (PDF1.2). This effect of low R:FR correlated with a reduced sensitivity to jasmonate (JA), thus resembling the antagonistic effects of salicylic acid (SA) on JA responses. Low R:FR failed to depress PDF1.2 mRNA levels in a transgenic line in which PDF1.2 transcription was up-regulated by constitutive expression of ERF1 in a coronatine insensitive1 (coi1) mutant background (35S::ERF1/coi1). These results suggest that the low R:FR effect, in contrast to the SA effect, requires a functional SCFCOI1-JASMONATE ZIM-DOMAIN (JAZ) JA receptor module. Furthermore, the effect of low R:FR depressing the JA response was conserved in mutants impaired in SA signaling (sid2-1 and npr1-1). Plant exposure to low R:FR ratios and the phyB mutation markedly increased plant susceptibility to B. cinerea; the effect of low R:FR was (1) independent of the activation of the shade-avoidance syndrome, (2) conserved in the sid2-1 and npr1-1 mutants, and (3) absent in two RNA interference lines disrupted for the expression of the JAZ10 gene. Collectively, our results suggest that low R:FR ratios depress Arabidopsis (Arabidopsis thaliana) immune responses against necrotrophic microorganisms via a SA-independent mechanism that requires the JAZ10 transcriptional repressor and that this effect may increase plant susceptibility to fungal infection in dense canopies.

Jasmonate-dependent and -independent pathways mediate specific effects of solar ultraviolet B radiation on leaf phenolics and antiherbivore defense.

Ultraviolet B (UV-B) radiation, a very small fraction of the daylight spectrum, elicits changes in plant secondary metabolism that have large effects on plant-insect interactions. The signal transduction pathways that mediate these specific effects of solar UV-B are not known. We examined the role of jasmonate signaling by measuring responses to UV-B in wild-type and transgenic jasmonate-deficient Nicotiana attenuata plants in which a lipoxygenase gene (NaLOX3) was silenced (as-lox). In wild-type plants, UV-B failed to elicit the accumulation of jasmonic acid (JA) or the bioactive JA-isoleucine conjugate but amplified the response of jasmonate-inducible genes, such as trypsin proteinase inhibitor (TPI), to wounding and methyl jasmonate, and increased the accumulation of several phenylpropanoid derivatives. Some of these phenolic responses (accumulation of caffeoyl-polyamine conjugates) were completely lacking in as-lox plants, whereas others (accumulation of rutin and chlorogenic acid) were similar in both genotypes. In open field conditions, as-lox plants received more insect damage than wild-type plants, as expected, but the dramatic increase in resistance to herbivory elicited by UV-B exposure, which was highly significant in wild-type plants, did not occur in as-lox plants. We conclude that solar UV-B (1) uses jasmonate-dependent and -independent pathways in the elicitation of phenolic compounds, and (2) increases sensitivity to jasmonates, leading to enhanced expression of wound-response genes (TPI). The lack of UV-B-induced antiherbivore protection in as-lox plants suggests that jasmonate signaling plays a central role in the mechanisms by which solar UV-B increases resistance to insect herbivores in the field.

UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation.

Light is emerging as a central regulator of plant immune responses against herbivores and pathogens. Solar UV-B radiation plays an important role as a positive modulator of plant defense. However, since UV-B photons can interact with a wide spectrum of molecular targets in plant tissues, the mechanisms that mediate their effects on plant defense have remained elusive. Here, we show that ecologically meaningful doses of UV-B radiation increase Arabidopsis resistance to the necrotrophic fungus Botrytis cinerea and that this effect is mediated by the photoreceptor UVR8. The UV-B effect on plant resistance was conserved in mutants impaired in jasmonate (JA) signaling (jar1-1 and P35S:JAZ10.4) or metabolism of tryptophan-derived defense compounds (pen2-1, pad3-1, pen2 pad3), suggesting that neither regulation of the JA pathway nor changes in levels of indolic glucosinolates (iGS) or camalexin are involved in this response. UV-B radiation, acting through UVR8, increased the levels of flavonoids and sinapates in leaf tissue. The UV-B effect on pathogen resistance was still detectable in tt4-1, a mutant deficient in chalcone synthase and therefore impaired in the synthesis of flavonoids, but was absent in fah1-7, a mutant deficient in ferulic acid 5-hydroxylase, which is essential for sinapate biosynthesis. Collectively, these results indicate that UVR8 plays an important role in mediating the effects of UV-B radiation on pathogen resistance by controlling the expression of the sinapate biosynthetic pathway.