Skip to main content
NCBI home page
Plant Signaling & Behavior logoLink to Plant Signaling & Behavior
. 2010 Nov 1;5(11):1504–1509. doi: 10.4161/psb.5.11.13705

Blue light photoreceptors are required for the stability and function of a resistance protein mediating viral defense in Arabidopsis

Rae-Dong Jeong 1, Aardr Kachroo 1, Pradeep Kachroo 1,✉
PMCID: PMC3115268  PMID: 21057210

Abstract

This light-perceiving ability of plants requires the activities of proteins termed photoreceptors. In addition to various growth and developmental processes, light also plays a role in plant defense against pathogens and is required for activation of several defense genes and regulation of the cell death response. However, the molecular or biochemical basis of light modulated regulation of defense signaling is largely unclear. We demonstrate a direct role for blue-light photoreceptors in resistance (R) protein-mediated plant defense against Turnip Crinkle Virus (TCV) in Arabidopsis. The blue-light photoreceptors, cryptochrome (CRY) 2 and phototropin (PHOT) 2, are specifically required for maintaining the stability of the R protein HRT, and thereby resistance to TCV. Exogenous application of the phytohormone salicylic acid elevates HRT levels in phot2 but not in cry2 background. These data indicate that CRY2 and PHOT2 function distinctly in maintaining post-transcriptional stability of HRT. HRT-mediated resistance is also dependent on CRY1 and PHOT1 proteins, but these do not contribute to the stability of HRT. HRT interacts with the CRY2/PHOT2-interacting protein COP1, a E3 ubiquitin ligase. Exogenous application of a proteasome inhibitor prevents blue-light-dependent degradation of HRT, suggesting that HRT is degraded via the 26S proteasome. These and the fact that PHOT2 interacts directly with the R protein RPS2 suggest that blue-light photoreceptors might be involved in regulation and/or signaling mediated by several R proteins.

Key words: Turnip Crinkle Virus, light, defense, blue-light, R protein, photoreceptors

Plants utilize both passive and active mechanisms to defend themselves against a constant barrage of potentially pathogenic microorganisms. Preformed physical and chemical barriers provide passive defense, while active mechanisms involve the production of antimicrobial compounds, cell wall reinforcement via the synthesis of lignin and callose, and the specific induction of elaborate defense signaling pathways. Recognition of pathogen-derived molecules can provide species level resistance to non-host pathogens, local and systemic resistance to race-specific pathogens, and basal resistance to virulent pathogens. Species-specific immunity is induced when a strain-specific avirulent (avr) protein from the pathogen associates directly/indirectly with a cognate plant resistance (R) protein, and is commonly called R-mediated resistance (reviewed in ref. 1).

Plant defense responses are modulated by a number of environmental factors, including light. For example, light induces the production of antimicrobial phytoalexins, and the expression of phytoalexin biosynthetic genes.2,3 Increasing evidence indicates that light is important for the proper induction of plant defense and for resistance to pathogens (reviewed in refs. 4 and 5). Mutations in genes encoding photoreceptors PHYA or PHYB compromise the ability to induce localized cell death at the site of pathogen entry.6 This phenomenon, termed the hypersensitive response (HR), is one of the earliest visible manifestations of induced defense signaling. In addition to HR development, the phyA and phyB mutants are also repressed in the salicylic acid (SA)-induced expression of the pathogenesis related (PR) gene, a molecular marker for the induction of SA responses. More recent analysis has suggested a major role for PHYA PHYB in systemic immunity and a rather minor role in local defense response.7

Light is also required for cell death and production of reactive oxygen species. The cell death phenotype of many lesion mimic mutants of Arabidopsis, maize, rice and soybean is dependent on light.8–13 Similar to cultured mammalian cells, exposure to blue and ultra violet light stimulates production of reactive oxygen species in aleurone protoplasts resulting in cell death.14 Similarly, light triggered production of excess porphyrin free radicals is responsible for cell death in maize plants mutated in the gene encoding uroporphyrinogen decarboxylase.15 Constitutive cell death in the defense-related Arabidopsis mutants, acd11 or vad1, as well as cell death induced in response to fungal toxins or viral infections is light dependent.16–20 Although these and many other examples have established a role for light in plant defense, the molecular and biochemical interaction between light and defense signaling pathways remains largely unclear.

Photoreceptors

The light-absorbing ability of plants is derived from the activities of three known classes of photoreceptors. These include phytochromes (PHY) that detect light in the red/far-red (600–700 nm) range and cryptochromes (CRY) and phototropins (PHOT) that detect light in the blue and UVA (320–500 nm) range. The Arabidopsis genome contains five genes encoding PHY proteins designated, PHYA, PHYB, PHYC, PHYD and PHYE; three genes encoding CRY proteins designated, CRY1, CRY2 and CRY3; two genes encoding PHOT proteins designated, PHOT1 and PHOT2 (reviewed in refs. 4, 5, 21–29).

Photon-activation converts the PHY proteins from their physiologically inactive to active far-red absorbing forms. Light also modulates the phosphorylation and nucleo-cytoplasmic translocation of PHY proteins, which is essential for their function in mediating light-responsive physiological changes in plants. CRY proteins are thought to have evolved from photolyases, but have no DNA-repair activity.25 CRY1 and CRY2 proteins are present in the nucleus/cytoplasm and are known to shuttle between these organelles. Recent work has shown that regulation of hypocotyl elongation and floral initiation requires nuclear localization of CRY2.30 The photon-excited CRY2 is phosphorylated in the nucleus and subsequently degraded. In contrast to CRY2, CRY1 is stable under continuous blue-light irradiation. Both CRY1 and CRY2 interact with the E3 ubiquitin ligase, COP1 (CONSTITUTIVELY PHOTO-MORPHOGENIC 1).31,32 Perception of blue-light by the CRY photoreceptors is thought to trigger rapid degradation of COP1 by an unknown mechanism. This results in the accumulation of the bZIP transcription factor, HY5 (ELONGATED HYPOCOTYL 5) and in turn the transcription of HY5 target genes.33 A basix-helix-loop-helix protein, which interacts with CRY2 in a blue-light specific manner and a serine/threonine protein phosphatase are two downstream signals identified in the CRY pathway.

PHOT proteins contain two LOV (light-oxygen-voltage) domains, LOV1 and LOV2 at the N-terminus and a serine/threonine kinase domain at the C-terminus (reviewed in refs. 24 and 26). In the dark, binding with LOV2 domain inhibits the phosphorylation activity of the kinase domain. Binding to LOV2 is inhibited in light resulting in activation of kinase activity. LOV1 domains in turn appear to serve as attenuators of LOV2-domain-induced kinase activity in light.34 The in planta substrates phosphorylated by PHOT proteins are not known. Both PHOT1 and PHOT2 are localized to the plasma membrane and autophosphorylation is thought to promote their dissociation from the plasma membrane.35–38 Upon blue-light irradiation, PHOT1 moves rapidly to the cytoplasm and a fraction of PHOT2 moves to the Golgi apparatus. The significance of this relocalization or autophosphorylation remains unclear. Two closely related PHOT1-interacting proteins, NPH (NONPHOTOTROPIC HYPOCOTYL) 3,39 and RPT (ROOT PHOTOTROPISM) 2,40 have been identified as possible downstream intermediates. Like, PHOT1, NPH3 is associated with the plasma membrane and is thought to serve as a scaffold to assemble components of a phototropin receptor complex. Interestingly, N-terminal of NPH3 and RPT2 bind to the N-terminal of PHOT1 but not of PHOT2 (reviewed in refs. 24 and 26).

Some of the blue-light photoreceptors are known to participate in plant defense or responses related to defense signaling. For example, programmed cell death in the presence of blue light requires the activation of CRY1.41 More recently, CRY1 was shown to positively regulate RPS2-mediated resistance and systemic acquired resistance (SAR) under continuous light.42 However, CRY1 is not required for RPS2-mediated resistance when plants are grown under 14 h light: 10 h dark photocycles. This suggests that photoreceptors function differently under different light conditions and/or that they play redundant roles in mediating bacterial resistance. This possibility is further supported by the fact that both PHOT1 and PHOT2 interacts directly with the R protein RPS2 (Fig. 1).43 Clearly, more work is required to elucidate the role(s) of PHY and blue-light photoreceptors in R protein-mediated resistance to bacterial pathogens.

Figure 1.

Figure 1

Open in a new tab

RPS2 interacts with PHOT2. Confocal micrographs showing bimolecular fluorescence complementation for RPS2 and PHOT2. Agroinfiltration was used to express protein in transgenic Nicotiana benthamiana plants expressing the nuclear marker CFP-H2B. The merged micrographs are CFP and YFP overlay images. The arrow indicates nucleus.

The Arabidopsis-TCV Pathosystem

TCV is a small icosahedral virus belonging to the carmovirus group. Its 4 kb genome consists of a single-stranded, positive-sense RNA and encodes five open reading frames. Except Di (Dijon)-17, most other Arabidopsis ecotypes are susceptible to TCV (Dempsey et al. 1997). Following TCV infection, Di-17 plants develop HR, express several defense genes, including PR (PATHOGENESIS RELATED)-1, PR-2, PR-5 and GST1 (GLUTATHIONE-S-TRANSFERASE 1) and accumulate SA.44,45 In contrast, susceptible plants fail to develop HR, after TCV infection; do not induce PR or GST1 gene expression and do not accumulate increased levels of SA. The susceptible genotypes also allow systemic spread of the virus, which is associated with a crinkled leaf and drooping bolt appearance, followed by death of the plant.44–47

HR to TCV is conferred by the dominant gene, HRT, which encodes a coiled coil (CC)-nucleotide binding site (NBS)-leucin rich repeat (LRR) protein with ∼90% identity to its paralogs RPP8 and RCY1 conferring resistance to Hyaloperonospora arabidopsidis Emco5 and Cucumber Mosaic Virus (CMV), respectively.46–50 In addition to its role in HR, HRT is required for resistance to TCV. However, HRT alone is not sufficient to confer TCV resistance, since all F1 plants and ∼75% of HR-developing F2 plants derived from a cross between resistant (Di-17) and susceptible (Col-0) ecotypes succumb to disease. Furthermore, ∼90% of transgenic Col-0 plants expressing the HRT transgene are susceptible to TCV even though these plants develop HR upon TCV inoculation.49,51 Subsequent studies showed that the recessive allele of a second, as yet unidentified locus, designated rrt (regulates resistance to TCV), is also required for resistance.45,51–53 The coat protein (CP) of the virus serves as the avirulence determinant on HRT rrt plants,49,54,55 although a direct interaction between HRT and TCV-CP has not been detected.51,56 Interestingly, TCV-CP was found to directly interact with a NAC transcription activator-like protein, TIP (TCV interacting protein) from Arabidopsis and inhibit the nuclear localization of TIP.57,58 Thus, it was suggested that HRT-mediated signaling is activated when interaction with TCV-CP alters the cellular distribution of TIP. However, this is unlikely because no interaction between HRT and TIP has been detected and more importantly, loss of TIP does not inhibit HRT rrt-mediated resistance to TCV.59

The requirement of rrt for resistance can be overcome by increasing the levels of HRT transcript via exogenous application of SA.52 Both HR and resistance are dependent upon SA, but do not require a key regulator of SA signaling, NPR1 (non-expressor of PR145,60). SA appears to function downstream of the recognition of TCV-CP by HRT and cannot confer resistance in the absence of HRT.52,53 We have shown that HRT rrt-mediated resistance to TCV is independent of RAR1, SGT1 and NDR1, but requires EDS1 and PAD4 (Fig. 2).52 A requirement for EDS1 in HRT-mediated resistance is rather atypical considering EDS1 was thought to function downstream of R proteins that contained toll-interleukin-like domain at their N terminal ends.61 Recent work has clarified that EDS1 and SA have redundant functions and thus a requirement for EDS1 is only evident when both SA and EDS1 are absent.62 For instance, absence of both EDS1 and SA is required to compromise HR to TCV as well as result in increased accumulation of virus62 (Fig. 2).

Figure 2.

Figure 2

Open in a new tab

A sketch of components involved in HRT-mediated resistance signaling pathway. TC V-induced resistance response is initiated upon indirect interaction between the dominant resistance protein HRT and TCV's avirulence factor, the coat protein (CP). Upon recognition of the pathogen, an HRT-mediated response leads to HR, accumulation of SA and PR-1 gene expression. Mutations in EDS1, PAD4, EDS5 and SID2 genes do not compromise HR or PR-1 expression. However, mutation in EDS1 and lack of SA compromises both HR to TCV and associated induction of PR-1 gene. Resistance to TCV is dependent on EDS1, PAD4, EDS5 and SID2 genes. Exogenous application of SA upregulates expression of the HRT and this step is mediated via PAD4 (dash and dotted line). Exogenous application of SA also upregulates expression of EDS1, PAD4 and PR-1 genes. Absence of light abolishes both HR and resistance to TCV and this in turn is associated with degradation of HRT. HRT interacts with COP1, an E3 ubiquitin ligase. Under normal light conditions, CRY2 and PHOT2 repress COP1-derived degradation of HRT by negatively regulating COP1. Degradation of CRY2 relieves the repression of COP1 activity and results in degradation of HRT.

Role of Light in Arabidopsis-TCV Interaction

Previously, we demonstrated a role for light in mediating HR and resistance to TCV.63 Absence of light significantly reduced the extent of HR formation in Di-17 plants after TCV inoculation and Di-17 plants exposed to 48 or 72 h of darkness post TCV inoculation showed a drastic decline in PR-1 gene expression. Furthermore, dark-treatment enhanced susceptibility in Di-17 plants such that plants maintained in 48 or 72 hours of darkness were ∼90% or 100% susceptible, respectively. Disease severity also increased with increase in the duration of the dark treatment. In comparison to Di-17, Col-0 plants subjected to varying lengths of dark periods did not exhibit alterations in disease symptoms, suggesting that light affects R-mediated resistance but not basal resistance to TCV. We also showed that increasing the length of the dark phase post TCV inoculation affected the accumulation of TCV-induced SA-glucoside (SAG), but not SA. However, reduced SAG accumulation was likely not responsible for the enhanced susceptibility of the dark-treated Di-17 plants, since SAG is biologically inactive. No change in SA/SAG levels was observed in Col-0 plants. Concurrent to the results with dark-treated plants, Di-17 plants subjected to varying lengths of light before dark treatment showed a progressive increase in resistance upto 12 h of light before dark. This suggested that increasing the length of the light phase immediately after TCV inoculation increased the number of resistant plants proportionately. However, resistance was reduced in plants that were exposed to extended periods of light before a dark cycle in comparison to plants exposed to normal day/night conditions. Thus, a light phase followed by a dark phase is likely essential for an optimal resistance response.

Interestingly, treatment with SA prior to TCV inoculation enhanced resistance in dark-treated Di-17 plants. However, SA enhanced resistance only if applied in advance of, but not together with dark treatment. This indicated that light is required to trigger SA-mediated signaling. Consistent with this data, plants treated with the SA analog BTH did not induce PR-1 gene expression when incubated in the dark. As expected, BTH treatment did not alter resistance in Col-0 plants irrespective of light conditions. These data suggest that pre-induction of the SA pathway in the presence of light might provide factor(s) that are required for HRT-mediated resistance. Interestingly, absence of light did not appear to alter TCV-induced activation of other defense responses such as the TCV-induced accumulation of free SA, or basal expression of HRT in uninoculated Di-17 plants.

To elucidate the precise role of light in signaling mediated by the R protein HRT, epitope (FLAG)-tagged HRT was expressed under its native promoter in Di-17 (HRT rrt, resistant) and Col-0 (hrt RRT, susceptible) ecotypes. TCV inoculation of the Col-0 HRT-FLAG lines induced HR formation and PR-1 gene expression similar to that in Di-17 or Di-17 HRT-FLAG plants indicating that the HRT-FLAG fusion protein was functional. Consistent with the requirement of rrt for TCV resistance, Col-0 HRT-FLAG lines remained susceptible to TCV. A comparison of HRT-FLAG levels and localization in Di-17 HRT-FLAG plants incubated under normal photoperiod (14 h light, 10 h dark) versus those incubated in darkness showed reduced levels of HRT in dark-treated plants. This indicated that the dark-induced susceptibility in Di-17 plants was likely due to reduction in HRT levels. HRT was found to be a peripheral plasma membrane associated protein, whose levels and sub-cellular localization did not change in response to TCV inoculation.51

Since light perception is mediated via the activities of photoreceptors, epistatic mutant analysis was carried out to determine the roles of the various photoreceptors in HRT-mediated resistance. The phyA, phyB, phyC, phyD, phyE, cry1, cry2, phot1, phot2, or the phyA phyB double mutations were mobilized in the Di-17 background and F2 progeny homozygous for the mutant allele and containing at least one copy of HRT were tested for HR development and resistance to TCV. Our analysis showed that HRT-mediated resistance is neither altered in the phyC, phyD, phyE single mutants, nor the phyA phyB double mutant. In contrast, mutations in cry1, cry2, phot1 or phot2 abrogate HRT-mediated resistance; all plants containing HRT and mutant cry1, cry2, phot1 or phot2 loci were susceptible. This indicated that blue-light photoreceptors are required for HRT-mediated resistance.51

Analysis of protein levels in cry1, cry2, phot1 or phot2 plants expressing the HRT-FLAG gene showed that levels of the HRT-FLAG protein were significantly reduced in HRT cry2 and HRT phot2 plants, but not in HRT cry1 or HRT phot1 plants. Reduced protein levels were not attributable to transcript instability because the HRT cry2 or HRT phot2 plants contained wild-type levels of the HRT-FLAG transcript. Thus, the CRY2 and PHOT2 proteins likely contribute to HRT-mediated resistance by affecting the stability of the HRT protein, whereas CRY1 and PHOT1, which are not essential for HRT stability, likely function elsewhere in the signaling pathway. Interestingly, HRT levels were not completely abolished in HRT cry2 or HRT phot2 plants such that residual levels of the protein were sufficient for inducing normal HR to TCV in these plants. Similar to wild-type plants, TCV inoculation did not alter HRT levels in cry1, cry2, phot1 or phot2 backgrounds.51

Exogenous SA, which enhances resistance to TCV by inducing HRT transcription,51–53 induced HRT protein levels in Di-17, HRT cry1, HRT phot1 and HRT phot2, but not HRT cry2 plants. Consistently, SA treatment enhanced resistance to TCV only in HRT cry1, HRT phot1 and HRT phot2 plants and not in HRT cry2 plants. Thus, increased expression of the HRT transcript is able to compensate for the lack of CRY1, PHOT1 and PHOT2 proteins but not for the absence of the CRY2 protein. Interestingly, HRT cry1 (wild-type levels of HRT protein) and HRT cry2 (low HRT protein) plants accumulated similar levels of SA and only marginally lower levels of SAG, as wild-type (Di-17) plants. On the other hand, HRT phot1 (wild-type HRT protein) and HRT phot2 (low HRT protein) plants did accumulate significantly lower levels of SA/SAG, indicating that the phot1 mutation likely impaired resistance by compromising SA synthesis. However, no direct correlation between the levels of TCV-induced SA and HRT protein could be established in the various mutant backgrounds.

Blue light degrades CRY2 and thereby HRT.

We observed that dark treatment also lowered the levels of CRY2, but not CRY1, PHOT1 or PHOT2.51 Consistent with blue-light triggered degradation of CRY2,64,65 levels of HRT-FLAG were significantly reduced within 6 h of blue-light treatment. Notably, reduction in HRT levels was quicker (within 6 h) than that of CRY2, suggesting that a certain threshold level of CRY2 might be required for the stability of HRT. Consistent with the degradation of HRT, the Di-17 HRT-FLAG plants exposed to blue-light showed susceptibility to TCV and supported the systemic movement of the virus. Interestingly and unlike the cry2 mutant plants, plants exposed to blue-light were also compromised in HR to TCV.51

CRY2 and PHOT2 did not contribute to HRT stability via direct interactions with the R protein. Interestingly, HRT interacted with the CRY2- and PHOT2-interacting protein, COP1, in both bimolecular fluorescence complementation assays and co-immunoprecipitation assays. HRT did not interact with another CRY2-interacting protein, CIB1. COP1, an E3 ubiquitin ligase, is involved in protein degradation via the 26S proteasome. We therefore examined the effects of the 26S proteasome-specific inhibitor MG132 on blue-light-dependent HRT degradation. Pretreatment with MG132 significantly inhibited the blue light-mediated degradation of the HRT-FLAG protein. Consistent with this result, plants exposed to blue-light showed resistance to TCV when pretreated with MG132.

These results have led to the hypothesis that under normal light conditions, CRY2 and/or PHOT2 repress COP1-derived degradation of HRT levels via direct interactions with COP1.29 In the dark, or under blue-light conditions, CRY2 degradation and possible conformational changes in PHOT2 relieve the repression of COP1 activity. This enables COP1 to interact with HRT and thereby targets HRT for degradation. Our immediate interests are to test the precise role of COP1 in blue light-mediated degradation of HRT and identify factors involved in CRY2/PHOT2-mediated regulation of HRT stability and resistance to TCV.

Acknowledgements

This work was supported by grants from the National Science Foundation (IOS#0641576) and Kentucky Science and Engineering Foundation (555-RDE-005).

Addendum to: Jeong RD, Chandra-Shekara AC, Barman S, Navarre D, Klessig D, Kachroo A, Kachroo P. CRYPTOCHROME 2 and PHOTOTROPIN 2 regulate resistance protein mediated viral defense by negatively regulating a E3 ubiquitin ligase. Proc Natl Acad Sci USA. 2010;107:13538–13543. doi: 10.1073/pnas.1004529107.

Footnotes

References

  • 1.Eitas T, Dangl JD. NB-LRR proteins: pairs, pieces, perception, partners and pathways. Curr Opin Plant Biol. 2010;13:4727. doi: 10.1016/j.pbi.2010.04.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Graham TL, Graham MY. Signaling in soybean phenylpropanoid responses (dissection of primary, secondary and conditioning effects of light, wounding and elicitor treatments) Plant Physiol. 1996;110:1123–1133. doi: 10.1104/pp.110.4.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Douglas CJ, Hauffe KD, Ites-Morales ME, Ellard M, Paszkowski U, Hahlbrock K, et al. Exonic sequences are required for elicitor and light activation of a plant defense gene, but promoter sequences are sufficient for tissue specific expression. EMBO J. 1991;10:1767–1775. doi: 10.1002/j.1460-2075.1991.tb07701.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Karpinski S, Gabrys H, Mateo A, Karpinska B, Mullineaux P. Light perception in plant disease defense signaling. Curr Opin Plant Biol. 2003;6:390–396. doi: 10.1016/s1369-5266(03)00061-x. [DOI] [PubMed] [Google Scholar]
  • 5.Roberts MR, Paul ND. Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defense against pests and pathogens. New Phytologist. 2006;170:677–699. doi: 10.1111/j.1469-8137.2006.01707.x. [DOI] [PubMed] [Google Scholar]
  • 6.Genoud T, Buchala AJ, Chua NH, Metraux JP. Phytochrome signalling modulates the SA-perceptive pathway in Arabidopsis. Plant J. 2002;31:87–95. doi: 10.1046/j.1365-313x.2002.01338.x. [DOI] [PubMed] [Google Scholar]
  • 7.Griebel T, Zeier J. Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defence. Plant Physiol. 2008;147:790–801. doi: 10.1104/pp.108.119503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Fuse T, Iba K, Satoh H, Nishimura M. Characterization of a rice mutant having an increased susceptibility to light stress at high temperature. Physiol Plant. 1993;89:799–804. [Google Scholar]
  • 9.Gray J, Janick-Buckner D, Close PS, Johal GS. Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol. 2002;130:1894–1907. doi: 10.1104/pp.008441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Hu G, Yalpani N, Briggs SP, Johal GS. A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell. 1998;10:1095–1105. doi: 10.1105/tpc.10.7.1095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Jabs T, Dietrich RA, Dangl JL. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996;273:1853–1856. doi: 10.1126/science.273.5283.1853. [DOI] [PubMed] [Google Scholar]
  • 12.Kim HK, Kim YJ, Paek KH, Chung JJ, Kim JK. The phenotype of the soybean disease-lesion mimic (dlm) mutant is light-dependent and associated with chloroplast function. Plant Pathol J. 2005;21:395–401. [Google Scholar]
  • 13.Mach JM, Castillo AR, Hoogstraten R, Greenberg JT. The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc Natl Acad Sci USA. 2001;98:771–776. doi: 10.1073/pnas.021465298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Bethke PC, Jones RL. Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J. 2001;25:19–29. doi: 10.1046/j.1365-313x.2001.00930.x. [DOI] [PubMed] [Google Scholar]
  • 15.Hu G, Yalpani N, Briggs SP, Johal GS. A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell. 1998;10:1095–1105. doi: 10.1105/tpc.10.7.1095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Allen LJ, MacGregor KB, Koop RS, Bruce DH, Karner J, Bown AW. The relationship between photosynthesis and a mastoparan-induced hypersensitive response in isolated mesophyll cells. Plant Physiol. 1999;119:1233–1242. doi: 10.1104/pp.119.4.1233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, et al. Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene- and salicylate-dependent signaling pathways. Plant Cell. 2000;12:1823–1836. doi: 10.1105/tpc.12.10.1823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Brodersen P, Petersen M, Pike HN, Olszak B, Skov-Petersen S, Oedum N, et al. Knockout of Arabidopsis ACCELERATED-CELL-DEATH11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev. 2002;16:490–502. doi: 10.1101/gad.218202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Lorrain S, Lin B, Auriac MC, Kroj T, Saindrenan P, Nicole M, et al. VASCULAR ASSOCIATED DEATH1, a novel GRAM domain-containing protein, is a regulator of cell death and defense responses in vascular tissues. Plant Cell. 2004;16:2217–2232. doi: 10.1105/tpc.104.022038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J. 2007;51:941–954. doi: 10.1111/j.1365-313X.2007.03191.x. [DOI] [PubMed] [Google Scholar]
  • 21.Casal JJ. Phytochromes, cryptochromes, phototropin: Photoreceptor interactions in plants. Photochem and Photobiol. 2000;71:1–11. doi: 10.1562/0031-8655(2000)071<0001:pcppii>2.0.co;2. [DOI] [PubMed] [Google Scholar]
  • 22.Cashmore AR. Cryptochromes: Enabling plants and animals to determine circadian time. Cell. 2003;114:12142–12147. [PubMed] [Google Scholar]
  • 23.Chen M, Chory J, Fankhauser C. Light signal transduction in higher plants. Annu Rev Genet. 2004;38:87–117. doi: 10.1146/annurev.genet.38.072902.092259. [DOI] [PubMed] [Google Scholar]
  • 24.Christie JM. Phototropin blue-light photoreceptors. Annu Rev Plant Biol. 2007;58:21–45. doi: 10.1146/annurev.arplant.58.032806.103951. [DOI] [PubMed] [Google Scholar]
  • 25.Gyula P, Schafer E, Nagy F. Light perception and signaling in higher plants. Curr Opin Plant Biol. 2003;6:446–452. doi: 10.1016/s1369-5266(03)00082-7. [DOI] [PubMed] [Google Scholar]
  • 26.Kimura M, Kagawa T. Phototropin and light-signaling in phototropism. Curr Opin Plant Biol. 2006;9:503–508. doi: 10.1016/j.pbi.2006.07.003. [DOI] [PubMed] [Google Scholar]
  • 27.Lin C, Shalitin D. Cryptochrome structure and signal transduction. Annu Rev Plant Biol. 2003;54:469–496. doi: 10.1146/annurev.arplant.54.110901.160901. [DOI] [PubMed] [Google Scholar]
  • 28.Liscum E. “The Arabidopsis Book”. Rockville, MD: American Society of Plant Biologists; 2000. Phototropism: Mechanisms and outcomes. [DOI] [Google Scholar]
  • 29.Lau OS, Deng XW. Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol. 2010;13:1–7. doi: 10.1016/j.pbi.2010.07.001. [DOI] [PubMed] [Google Scholar]
  • 30.Yu X, Klejnot J, Zhao Z, Shalitin D, Maymon M, Yang H, et al. Arabidopsis cryptochrome 2 completes its posttranslational life cycle in nucleus. Plant Cell. 2007;19:3146–3156. doi: 10.1105/tpc.107.053017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Wang H, Ma LG, Li JM, Zhao HY, Deng XW. Direct interaction of Arabidopsis crytochromes with COP1 in light control development. Science. 2001;294:154–158. doi: 10.1126/science.1063630. [DOI] [PubMed] [Google Scholar]
  • 32.Yang HQ, Tang RH, Cashmore AR. The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell. 2001;13:2573–2587. doi: 10.1105/tpc.010367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Hardtke CS, Gohda K, Osterlund MT, Oyama T, Okada K, Deng XW. HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J. 2000;19:4997–5006. doi: 10.1093/emboj/19.18.4997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Matsuoka D, Tokutomi S. Blue light-regulated molecular switch of Ser/Thr kinase in phototropin. Proc Natl Acad Sci USA. 2005;102:13337–13342. doi: 10.1073/pnas.0506402102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Sakamoto K, Briggs W. Cellular and subcellular localization of phototropin 1. Plant Cell. 2000;14:1723–1735. doi: 10.1105/tpc.003293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Kong SG, Suzuki T, Tamura K, Mochizuki N, Hara-Nishimura I, Nagatani A. Blue light-induced association of phototropin 2 with the golgi apparatus. Plant J. 2006;45:994–1005. doi: 10.1111/j.1365-313X.2006.02667.x. [DOI] [PubMed] [Google Scholar]
  • 37.Inoue SI, Kinoshita T, Matsumoto M, Nakayama KI, Doi M, Shimazaki KI. Blue light-induced autophosphorylation of phototropin is a primary step for signaling. Proc Natl Acad Sci USA. 2008;105:5626–5631. doi: 10.1073/pnas.0709189105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Wan YL, et al. The subcellular localization of blue-light induced movement of phototropin 1-GFP in etiolated seedlings of Arabidopsis thaliana. Mol Plant. 2008;1:103–117. doi: 10.1093/mp/ssm011. [DOI] [PubMed] [Google Scholar]
  • 39.Motchoulski A, Liscum E. Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. Science. 1999;286:961–964. doi: 10.1126/science.286.5441.961. [DOI] [PubMed] [Google Scholar]
  • 40.Sakai T, Wada T, Ishiguro S, Okada K. RPT2: A signal transducer of the phototropic response in Arabidopsis. 2000;12:225–236. doi: 10.1105/tpc.12.2.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Danon A, Coll NS, Apel K. Cryptochrome-1-dependent execution of programmed cell death induced by singlet oxygen in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2006;103:17036–17041. doi: 10.1073/pnas.0608139103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Wu L, Yang HQ. CRYPTOCHROME 1 is implication in promoting R protein-mediated plant resistance to Pseudomonas syringae in Arabidopsis. Mol Plant. 2010;3:539–548. doi: 10.1093/mp/ssp107. [DOI] [PubMed] [Google Scholar]
  • 43.Qi Y, Katagiri F. Purification of low-abundance Arabidopsis plasma-membrane protein complexes and identification of candidate components. Plant J. 2008;57:932–944. doi: 10.1111/j.1365-313X.2008.03736.x. [DOI] [PubMed] [Google Scholar]
  • 44.Dempsey DA, Wobbe KK, Klessig DF. Resistance and susceptible responses of Arabidopsis thaliana to turnip crinkle virus. Phytopathol. 1997;83:1021–1029. [Google Scholar]
  • 45.Kachroo P, Yoshioka K, Shah J, Dooner HK, Klessig DF. Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes, is salicylic acid dependent but NPR1, ethylene and jasmonate independent. Plant Cell. 2000;12:677–690. doi: 10.1105/tpc.12.5.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Kachroo P. In: Natural Resistance Mechanisms of Plants to Viruses. Loebenstein G, Carr JP, editors. Dordrecht, The Netherlands: Kluwer Academic Publishers; 2006. pp. 81–105. [Google Scholar]
  • 47.Kachroo P, Chandra-Shekara AC, Klessig D. Plant signal transduction and defense against viral pathogens. In: Maramososch K, Shatkin AJ, editors. Advances in Viral Research. Vol. 66. San Diego, CA: Academic Press; 2006. pp. 161–191. [DOI] [PubMed] [Google Scholar]
  • 48.McDowell JM, Dhandaydham M, Long TA, Aarts MG, Goff S, Holub EB, et al. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell. 1998;10:1861–1874. doi: 10.1105/tpc.10.11.1861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF. Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell. 2000;12:663–676. doi: 10.1105/tpc.12.5.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Takahashi H, Miller J, Nozaki Y, Takeda M, Shah J, Hase S, et al. RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J. 2002;32:655–667. doi: 10.1046/j.1365-313x.2002.01453.x. [DOI] [PubMed] [Google Scholar]
  • 51.Jeong RD, Chandra-Shekara AC, Barman SR, Navarre DA, Klessig D, Kachroo A, et al. CRYPTOCHROME 2 and PHOTOTROPIN 2 regulate resistance protein mediated viral defense by negatively regulating a E3 ubiquitin ligase. Proc Natl Acad Sci USA. 2010;107:13538–13543. doi: 10.1073/pnas.1004529107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Chandra-Shekara AC, Navarre D, Kachroo A, Kang HG, Klessig D, Kachroo P. Signaling requirements and role of salicylic acid in HRT- and rrt-mediated resistance to turnip crinkle virus in Arabidopsis. Plant J. 2004;40:647–659. doi: 10.1111/j.1365-313X.2004.02241.x. [DOI] [PubMed] [Google Scholar]
  • 53.Chandra-Shekara AC, Venugopal SC, Barman SR, Kachroo A, Kachroo P. Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis. Proc Natl Acad Sci USA. 2007;104:7277–7282. doi: 10.1073/pnas.0609259104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Oh JW, Kong W, Song C, Carpenter CD, Simon AE. Open reading frames of turnip crinkle virus involved in satellite symptom expression and incompatibility with Arabidopsis thaliana ecotype Dijon. Mol Plant-Microbe Interact. 1995;8:979–987. doi: 10.1094/mpmi-8-0979. [DOI] [PubMed] [Google Scholar]
  • 55.Wang J, Simon AE. Symptom attenuation by a satellite RNA in vivo is dependent on reduced levels of virus coat protein. Virology. 1999;259:234–245. doi: 10.1006/viro.1999.9781. [DOI] [PubMed] [Google Scholar]
  • 56.Kang HG, Kuhl JC, Kachroo P, Klessig DF. Turnip Crinkle Virus resistance in Arabidopsis requires CRT1, a new member of GHKL ATPase family. Cell Host Microbe. 2008;3:48–57. doi: 10.1016/j.chom.2007.11.006. [DOI] [PubMed] [Google Scholar]
  • 57.Ren T, Qu F, Morris TJ. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell. 2000;12:1917–1926. doi: 10.1105/tpc.12.10.1917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Ren T, Qu F, Morris TJ. The nuclear localization of the Arabidopsis transcription factor TIP is blocked by its interaction with the coat protein of Turnip crinkle virus. Virology. 2005;331:316–324. doi: 10.1016/j.virol.2004.10.039. [DOI] [PubMed] [Google Scholar]
  • 59.Jeong RD, Chandra-Shekara AC, Kachroo A, Klessig DF, Kachroo P. HRT-mediated hypersensitive response and resistance to Turnip crinkle virus in Arabidopsis does not require the function of TIP, the presumed guardee protein. Mol Plant Microbe Interact. 2008;21:1316–1324. doi: 10.1094/MPMI-21-10-1316. [DOI] [PubMed] [Google Scholar]
  • 60.Cao H, Bowling SA, Gordon AS, Dong X. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell. 1994;11:1583–1592. doi: 10.1105/tpc.6.11.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci USA. 1998;95:10306–10311. doi: 10.1073/pnas.95.17.10306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Venugopal SC, Jeong RD, Zhu S, Chandra-Shekara AC, Navarre D, Kachroo A, Kachroo P. ENHANCED DISEASE SUSCEPTIBILITY 1 and salicylic acid act redundantly to regulate resistance gene expression and low OLEATE-induced defense signaling. PLOS Genet. 2009;5:1000545. doi: 10.1371/journal.pgen.1000545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Chandra-Shekara AC, Gupte M, Navarre D, Raina S, Raina R, Klessig D, et al. Light-dependent hypersensitive response and resistance signaling against Turnip Crinkle Virus in Arabidopsis. Plant J. 2007;45:320–334. doi: 10.1111/j.1365-313X.2005.02618.x. [DOI] [PubMed] [Google Scholar]
  • 64.Ahmad M, Jarillo JA, Cashmore AR. Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability. Plant Cell. 1998;10:197–207. doi: 10.1105/tpc.10.2.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Lin C, Yang H, Guo H, Mockler T, Chen J, Cashmore AR. Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc Natl Acad Sci USA. 1998;95:2686–2690. doi: 10.1073/pnas.95.5.2686. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Signaling & Behavior are provided here courtesy of Taylor & Francis

RESOURCES