Characterization of temperature and light effects on the defense response phenotypes associated with the maize Rp1-D21autoactive resistance gene
- Adisu Negeri†1,
- Guan-Feng Wang†1,
- Larissa Benavente2,
- Cromwell M Kibiti3,
- Vijay Chaikam3,
- Guri Johal3 and
- Peter Balint-Kurti1, 2Email author
© Negeri et al.; licensee BioMed Central Ltd. 2013
Received: 22 September 2012
Accepted: 12 July 2013
Published: 26 July 2013
Rp1 is a complex locus of maize, which carries a set of genes controlling race-specific resistance to the common rust fungus, Puccinia sorghi. The resistance response includes the “Hypersensitive response” (HR), a rapid response triggered by a pathogen recognition event that includes localized cell death at the point of pathogen penetration and the induction of pathogenesis associated genes. The Rp1-D21gene is an autoactive allelic variant at the Rp1 locus, causing spontaneous activation of the HR response, in the absence of pathogenesis. Previously we have shown that the severity of the phenotype conferred by Rp1-D21 is highly dependent on genetic background.
In this study we show that the phenotype conferred by Rp1-D21 is highly dependent on temperature, with lower temperatures favoring the expression of the HR lesion phenotype. This temperature effect was observed in all the 14 genetic backgrounds tested. Significant interactions between the temperature effects and genetic background were observed. When plants were grown at temperatures above 30°C, the spontaneous HR phenotype conferred by Rp1-D21 was entirely suppressed. Furthermore, this phenotype could be restored or suppressed by alternately reducing and increasing the temperature appropriately. Light was also required for the expression of this phenotype. By examining the expression of genes associated with the defense response we showed that, at temperatures above 30°C, the Rp1-D21 phenotype was suppressed at both the phenotypic and molecular level.
We have shown that the lesion phenotype conferred by maize autoactive resistance gene Rp1-D21 is temperature sensitive in a reversible manner, that the temperature-sensitivity phenotype interacts with genetic background and that the phenotype is light sensitive. This is the first detailed demonstration of this phenomenon in monocots and also the first demonstration of the interaction of this effect with genetic background. The use of temperature shifts to induce a massive and synchronous HR in plants carrying the Rp1-D21 genes will be valuable in identifying components of the defense response pathway.
KeywordsMaize Hypersensitive response Disease resistance Temperature sensitive Light dependent Rp1 Autoactive R gene
The Rp1 locus of maize carries variable numbers of tandemly-repeated genes belonging to the nucleotide binding site, leucine-rich repeat (NB-LRR) class of major disease resistance genes (also known as R-genes; ) that confer race-specific resistance to the common rust fungus, Puccinia sorghi. The resistance response conferred by these genes is generally activated by a race-specific direct or indirect recognition of pathogen-derived molecules . It includes the “hypersensitive response” (HR) which is a rapid localized cell death at the point of pathogen penetration, the induction of pathogenesis associated genes and a variety of other responses .
The Rp1 locus is complex; the well characterized HRp1-D haplotype is composed of nine tandemly-repeated Rp1 paralogs  while the Rp1 haplotype of the B73 line carries four Rp1-homologous sequences  and more than 50 Rp1-homologous sequences have been identified in other lines . This complexity results in the locus being meiotically unstable [7, 8], with a high frequency of unequal crossover events . Intragenic recombination events resulting in the generation of chimeric genes derived from two different Rp1 paralogs have been observed several times. In some cases these lead to the generation of novel resistance specificities . In other cases it has led to the creation of dominant mutant genes that confer a “spontaneous necrotic” or “lesion” phenotype [10–13].
Rp1-D21 is one such gene . It confers a spontaneous lesion phenotype with lesions forming in apparently random locations without the requirement for the presence of a pathogen. Previously we showed that the Rp1-D21 phenotype is influenced by genetic background; in some backgrounds it is very severe, killing the plant during the juvenile phase. In others it is suppressed to the extent that the mutant plants can set seed in a more-or-less normal fashion [3, 14, 15].
The signal transduction pathway leading to the HR response and the mechanism by which the plant is able to restrict the HR to cells in the immediate area surrounding an infection is poorly understood in plants. We are using a series of genetic crosses with diverse lines and with members of segregating populations to identify loci and genes that interact with Rp1-D21 either to suppress or enhance its expression. The expectation is that many of these loci are also important in the regulation of the ‘normal’ HR induced by wild type R-genes in response to pathogen detection [3, 14, 15]. This approach, in which a mutant conferring an extreme phenotype in a trait of interest is used to uncover previously inaccessible genotype-dependent variation has been termed Mutant-Assisted Gene Identification and Characterization (MAGIC) [16, 17].
Temperature has long been known to play a role in the modulation of plant defense responses in dicots , including the HR [19–22]. In some cases it appears that the temperature-sensitive component of the defense response resides in the NB-LRR genes themselves . Light sensitivity of resistance responses, including HR, is likewise a well known phenomenon [24, 25]. In the course of our studies we noted that phenotypic expression of Rp1-D21 seemed to be affected by temperature. This effect had been briefly noted previously . In light of our ongoing work on the genetic dissection of HR using Rp1-D21 in a MAGIC approach, and especially because these experiments were taking place in multiple locations under varying environmental conditions, it was important to characterize this temperature-dependent effect further and to ascertain whether there was an interaction with genotype. We show here that while temperature effects on the Rp1-D21 phenotype were observed in all 14 genetic backgrounds tested, the temperature effects were significantly affected by genotype. The phenotype could be completely suppressed in a reversible way by manipulating temperature or light levels.
Results and discussion
Rp1-D21-associated lesion phenotypes are temperature dependent
The Rp1-D21-H95 line has the background of the common maize inbred H95 into which the Rp1-D21 allele has been introgressed. It is 97% genetically identical to H95 . Rp1-D21-H95 plants are heterozygous for the Rp1-D21 mutant allele and therefore the F1 progeny of any cross between Rp1-D21-H95 and another line segregate in a 1:1 ratio for F1 progeny carrying an Rp1-D21 gene (i.e. mutant F1 progeny) and F1 progeny carrying the wild-type (i.e. non-autoactive) H95 allele at the Rp1 locus (i.e. wild type F1 progeny). Importantly the wild type and mutant F1 progeny were almost entirely isogenic outside the Rp1 locus .
Mean lesion score (LES), and mean mutant to wild type height ratio (HTR) for crosses of various lines to Rp1-D21 -H95 grown under three different greenhouse temperature regimes
B97 × Rp1-D21-H95
CML103 × Rp1-D21-H95
CML228 × Rp1-D21-H95
CML277 × Rp1-D21-H95
CML322 × Rp1-D21-H95
Ky21 × Rp1-D21-H95
M162W × Rp1-D21-H95
M37W × Rp1-D21-H95
Mo18W × Rp1-D21-H95
MS-71 × Rp1-D21-H95
OH43 × Rp1-D21-H95
OH7B × Rp1-D21-H95
Tx303 × Rp1-D21-H95
The diversity of the Rp1-D21 mediated HR in maize [Adapted from Table 1 in reference 3]
B97 × Rp1-D21-H95
A632 × Rp1-D21-H95
Oh43 × Rp1-D21-H95
CML228 × Rp1-D21-H95
Mo18w × Rp1-D21-H95
Oh7B × Rp1-D21-H95
B73 × Rp1-D21-H95
CML333 × Rp1-D21-H95
Mo17 × Rp1-D21-H95
MS-71 × Rp1-D21-H95
CM103 × Rp1-D21-H95
CML277 × Rp1-D21-H95
Ky21 × Rp1-D21-H95
M162W × Rp1-D21-H95
M37W × Rp1-D21-H95
Tx303 × Rp1-D21-H95
ANOVA for lesion score (LES) and mutant to wild type height ratio (HTR) for 13 F 1 families derived diversity maize lines crossed to Rp1-D21 -H95 grown at three temperature ranges in two experiments during fall 2009 and fall 2010
Source of variance
Maize founder lines*Environment
Maize founder lines *temperature
Maize founder lines *temperature*Environment
Since LES and HTR measure aspects of the same phenotype, it was not surprising that they were highly correlated. Combined data from Fall 2009 and Fall 2010 showed strong negative phenotypic correlation between LES and HTR (Pearson correlation coefficient = -0.77, p < 0.001). At each temperature range the correlation was strong (Pearson correlation coefficient =-0.79, -0.78, and -0.44 at 18/22°C, 22/26°C, and 26/30°C, respectively). The correlation showed a trend of weakening association between LES and HTR as temperature increased. This was probably because higher temperature suppressed the phenotypic expression of the Rp1-D21 phenotype.
The effect of temperature reduction on the Rp1-D21-associated lesion phenotype
We subsequently conducted an experiment in which eight F1 seed from each of four families from the crosses of Rp1-D21-H95 to M37W, Tx303, M162W and B97, which represent a diversity of Rp1-D21supressive and enhancing backgrounds, were planted in growth chambers at 30/34°C (12 hours/12 hours)- i.e. 4°C higher than the HiGH. After three weeks growth at 30/34°C (~four leaf stage) no lesions were visible on any of the plants and it was impossible to discern wild type from mutant segregants. In one growth chamber the temperature was then dropped to 18/22°C. After 48 hours, half the plants (i.e. presumably the plants carrying the Rp1-D21 gene) from the M37W, Tx303, M162W F1 families developed copious lesions (an example is shown in Figure 2B). The plants from the B97 F1 family took longer to develop lesions but after seven days some lesions were visible on about half of the plants from this family too. In the growth chamber which had remained at 30/34°C all the plants still were indistinguishable from wild type and no lesions were visible on any leaves.
The HR-phenotype associated with Rp1-D21can be activated/inactivated reversibly using temperature shifts
At the four-week time point and using the same plants that had been shifted from 30/34°C to 18/22°C, the location at which the emerging leaves joined the main stem was marked on the mutant plants and the temperature of the growth chamber was increased from 18/22°C back to 30/34°C. After seven days, all the newly-emerged leaves and the newly-emerged portions of the leaves that had been partially emerged at four weeks showed no, or in just a few cases, a very few lesions (Figure 2C, D).
In a separate experiment (Additional file 2: Figure S2) we grew at least 3 mutant F1 plants from each of 13 different genotypes for four weeks at 22 /18°C and then shifted to 34/30°C. At this point the 5th leaves were partially emerged from the whorl. In every case a clear transition from a lesioned to a non-lesioned phenotype was apparent on the 5th leaf (Additional file 2: Figure S2).
This result implied two things: Firstly that the Rp1-D21 lesion phenotype could be turned off, then on, then off again simply by increasing the temperature above about 30°C and decreasing it to about 20°C by turns. In other words the activation/inactivation of the HR phenotype was reversible. Secondly, since no lesions were visible on portions of the plant that emerged immediately after the temperature was increased to 30/34°C, it implied that the Rp1-D21-associated lesions did not form before leaf emergence from the whorl but that something associated with leaf emergence, perhaps exposure to light, was required for the lesion phenotype.
An objectively measurable quantitative assay for Rp1-D21temperature-sensitive phenotype
To examine the detailed kinetics of Rp1-D21 lesion development following transfer to lower temperatures, four different genotypic combinations were selected: F1 progenies of Rp1-D21-H95 crossed to A632, B73, Mo17 and Tx303. The phenotype underlying Rp1-D21 is highly suppressed in a hybrid combination of H95 with A632, but highly enhanced in a hybrid combination with Tx303 while F1 hybrids of Rp1-D21-H95 with B73 and Mo17 exhibit intermediate phenotypes (Table 2).
Light requirement for Rp1-D21lesion manifestation
It should be noted that wrapping a portion of the leaf in aluminum foil as well as blocking out light, may have the effect of locally increasing the humidity and possibly also the temperature of the wrapped part of the leaf. So, conceivably, altered temperature and humidity might underlie the failure to form lesions. However, we have observed in other experiments that Rp1-D21 plants grown in bottles at ~100% humidity display characteristic lesions (data not shown). Therefore it seems that both light and a permissive temperature are required for Rp1-D21-associated lesions to form.
Temperature sensitivity of the defense response associated with Rp1-D21
While this is, to our knowledge the first detailed demonstration of this phenomenon in monocots, examples of temperature sensitive plant disease resistance genes have been long been known, with high temperatures often suppressing function . The tobacco N gene, which confers resistance to TMV and the Arabidopsis RPW8 gene, which confers resistance to powdery mildew are, like Rp1-D21, not effective above 30°C [27, 28]. Recently the temperature responses of two NB-LRR genes, the N gene and the Arabidopsis SNC1 gene, another NB-LRR gene associated with the defense response , were investigated. It was shown that the temperature sensitivity of the defense response they mediated was likely resided in the NB-LRR gene products themselves and not in some component of the downstream signal transduction pathway. Our work here further suggests that while the NBS-LRR gene product may be the primary cause of temperature-sensitivity the interaction of other loci and alleles can modulate this effect. Alcázar and Parker  reviewed the interaction of temperature and immune responsiveness in Arabidopsis (the system in which most of this work has been done). They suggest that temperature sensitivity might be a characteristic associated with the molecular assembly of which the NB-LRR gene is a part, but which also includes other proteins such as HSP90. They also suggest that, given the prevalence of this type of relationship, temperature sensitivity may have evolved as an adaptive strategy to ‘tune’ the defense response to the local environmental conditions to balance the advantages of a robust defense response (disease resistance) with the disadvantages such as reduced growth and reproductive potential [29, 30].
The basal defense response in Arabidopsis has been shown to be regulated in a circadian manner . The expression levels of several genes important for resistance to Hyaloperonospora arabidopsidis and for basal resistance were shown to peak around dawn, the time of peak spore dissemination. In this way, it was hypothesized, the plant was able to synchronize its maximal defense responsiveness to the period of maximal need. Of course dawn is also the coldest period of the day and so perhaps the temperature sensitivity of NB-LRR resistance complexes is another way of fine tuning this system. Similarly, light dependence of the HR mediated by other R-genes has been observed [24, 32]. In some cases, this may reflect a relationship between HR, photosynthesis and the oxidative balance in the cell [33, 34].
We have been using Rp1-D21 as a reporter for the HR in order to map loci important for controlling natural variation in the maize defense response [3, 14, 15]. This work is being performed largely in field experiments in North Carolina and Indiana. The results reported here suggest that environmental temperature will be an important factor in determining how severe the Rp1-D21 phenotype is in the field and, more importantly, that different temperatures may differentially affect different genotypes. This is not necessarily surprising. Genotype by environment interactions are observed in the vast majority of quantitative trait mapping studies, emphasizing the need for conducting studies over multiple environments.
The Rp1-D21 associated lesion phenotype is temperature-sensitive at both a morphological and a molecular level.
Rp1-D21 temperature-sensitivity is observed in all genetic backgrounds studied, including backgrounds that both strongly enhance and strongly suppress the phenotype.
However, there is a significant interaction between temperature and genotype. In other words, the response of the Rp1-D21 phenotype to changes in temperature is, in part, dependent on genetic background.
The effect of genotype on temperature sensitivity can be objectively quantified by examining the kinetics of lesion formation after temperature change.
The Rp1-D21 phenotype can be suppressed at temperatures above 30°C in all genetic backgrounds studied at both the gross phenotypic and the molecular level.
The Rp1-D21 phenotype can be suppressed and activated in a reversible manner by altering the external temperature.
Light exposure is also required for the Rp1-D21 lesion phenotype.
As noted above, temperature effects on the R-gene mediated defense response may be a general phenomenon in plants [18, 23, 35]. However this is the first time that the interaction of this effect with genetic background has been demonstrated. This implies that other genetic factors other than the R-gene itself are responsible for mediating the effect of temperature. Using the Rp1-D21 system and the MAGIC [14, 16, 17] technique we will now be able to examine the loci and genes underlying this response. Furthermore, the precise ability to turn the defense response on and off in a massive and synchronous way provides new resources with which to characterize the molecular and physiological events associated the maize defense response.
The Rp1-D21-H95 line was generated as described previously . Briefly, the Rp1-D21 variant was crossed to the maize inbred line H95, and subsequently backcrossed to the H95 parent four times, while selecting for the HR phenotype indicated by the spontaneous formation of cell death lesions. Since Rp1-D21 homozygotes in the H95 background are often unable to set seed, this stock is maintained in heterozygous condition by repeatedly crossing it as a male to the H95 inbred. A previous study showed that the Rp1-D21-H95 line is 97% identical genetically to H95 with 121.5 Mbp of the genome heterozygous for the recurrent and donor parent alleles out of a total genome size of 2045 Mbp . The Rp1-D21- B73 line was produced in the same way as Rp1-D21-H95, just substituting B73 for H95.
The Rp1-D21-H95 line was crossed to 13 diverse lines. All of these lines and B73 are among the 26 parents of the maize Nested Association Mapping population . F1 progenies segregated 1:1 mutant:wild type. Apart from the segregation of the Rp1-D21 gene, these progenies were essentially isogenic.
Plants were grown in the phytotron greenhouse facility at North Carolina State University with fixed temperatures of 22/18°C, 26/22°C, and 30/26°C higher/ lower for 12 hours each, respectively. For simplicity these greenhouses (GH) were referred to as LowGH, MidGH, and HiGH, respectively. In each year the experiment was laid out in randomized complete block design with two replicates per year per temperature condition. Within each replicate three wild type and three mutant plants were measured per genotype in 2009 and two plants per genotype in 2010. Each replicate was arranged as a randomized complete block. The experiment was performed in fall 2009 and fall 2010. No artificial lighting was used.
In each GH seeds were planted on a plastic germination tray. As soon as it was possible to distinguish wild types from mutant counterparts, seedlings were transplanted to a six inch pot with standard soil mix. Throughout the study period seedlings were watered two times a day on regular basis. Changes in growth and lesion development were photographed and documented.
For all the growth chamber experiments light level were maintained at approximately 325 micromoles/m/s using cool white fluorescent lights. Growth chamber experiments were performed to determine whether constant temperatures above 30°C could abrogate the expression of Rp1-D21 entirely and to determine whether the phenotype was reversible. Four F1 families: Tx303 × Rp1-D21-H95, M162W × Rp1-D21-H95, and M37W × Rp1-D21-H95, B97 × Rp1-D21-H95 were used for this experiment. In the first three of these F1 families, the Rp1-D21 phenotype is relatively enhanced; in the last it is relatively suppressed. The Rp1-D21-H95 and Rp1-D21-B73 lines were also included as standard checks for comparison. Eight plants were grown for each of the crosses in two growth chambers. Both growth chambers were initially calibrated at low temperature of 30°C and high temperature of 34°C. Illumation was fixed at 12 h dark and 12 h light and seedlings were regularly watered twice a day. In one growth chamber, after three weeks (corresponding to the four leaf stage), the temperature was changed to a low temperature of 18°C and high temperature of 22°C. After four weeks the temperature in this growth chamber was shifted back to 30/34°C. Temperature shifts took about 20 minutes to complete in every case. Light duration remained unchanged.
For the experiment to measure the kinetics of Rp1-D21-associated lesion formation, F1 crosses of Rp1-D21-H95 crossed to A632, B73, Mo17 and Tx303 were used. Twenty plants from each of the four F1 families cross were grown in pots (2 plants per pot) in a growth chamber under a daily photoperiod of 12 h. Initially the temperature of the growth chamber was maintained at a constant temperature of 30°C, but after 8-days of growth (V2 stage) the temperature was dropped to 26°C. Plants expressing HR lesions were counted twice every day for the next 9 days.
Phenotypic data collection
Plants were evaluated for a lesion severity phenotype on a 0–10 scale with 0 being no symptoms and 10 being dead. Wild type to mutant height ratio was also measured. This was simply the average height of the mutant plants divided by the average height of the wild type plants [3, 14]. Lesion severity was scored twice in both fall 2009 and fall 2010.
ANOVA was performed using SAS version 9.2 (SAS Institute, 2002–2008). SAS Version 9.2 PROC CORR (SAS Institute, 2002–2008) was used to estimate the Pearson correlation coefficients. Heritability estimates were calculated using PROC MIXED procedure of SAS, as described previously .
Total RNA was extracted from maize leaf tissue using Trizol (Life Technologies, Carlsbad, CA) according to manufacturer’s instructions. RNA concentration, quality and integrity were monitored by the NanoDrop and agarose gel electrophoresis. For cDNA synthesis, 1μg of total RNA was reverse transcribed using M-MLV (Life Technologies, Carlsbad, CA) following standard protocols. Briefly, total RNA was mixed with 1μl of Oligo (dT)20 primers (Life Technologies, Carlsbad, CA), heat denatured at 65°C for 5 min and chilled on ice for 2 min. To each reaction 4 μl of 5× First Strand buffer, 2 μl of 0.1 M DTT, and 1μl RNaseOUT (Life Technologies, Carlsbad, CA) was added. The reaction was incubated at 37°C for 2 min and then 1 μl of M-MLV was added, to a final volume of 20 μl. cDNA synthesis was performed at 37°C for 2 hours, followed by a 15 min incubation at 75°C for enzyme inactivation. The cDNA reaction was then diluted 5× using water.
The cDNAs were used for semi- quantitative measurements of gene expression using PCR. Primers PR1-F (5′-AGGCTCGCGTGCCTCCTAGCTCTGG-3′) and PR1-R (5′-GGAGTCGCGCCACACCACCTGCGTG-3′), PRms-F (5′-ACCTGGAGCACGAAGCTGCAG-3′) and PRms-R (5′-GCAGCCGATGCTTGTAGTGGC-3′), WIP1-F (5′-TGCTGATCCTGTGCCTCCAG-3′) and WIP1-R (5′-CTCTCTGATCTAGCACTTGGGG-3′) were utilized to amplify the maize defense genes PR1, PRms and WIP1, respectively . The maize genes EF1α and GAPDH2 were used as reference and amplified using primers EF1a-F1 (5’- ATCTGAAGCGTGGGTATGTG-3’) and EF1a-R1 (5’- GCATAGCCATTGCCAATCTG-3’) and GAPDH2-F2 (5’- GACTTCCTTGGTGACAGCAGG-3’) and GAPDH2-R2 (5’- CTGTAGCCCCACTCGTTGTC-3’), respectively. The EF1a and GAPDH2 primers were from Hachez et al.  and slightly modified as needed to minimize dimer formation. Amplification conditions consisted of 32 cycles of 94° for 30 sec, 57° for 30 sec, and 72° for 30 sec, using 250 uM of each primer and 1–4 uL of the 5× diluted cDNA reaction. All primers were obtained from Sigma-Aldrich (St. Louis, MO). Amplification products were analyzed by agarose gel electrophoresis. Genomic DNA contamination was monitored by the size of the amplification product for the GAPDH gene using B73 genomic DNA as positive control for the PCR.
This work was funded by USDA-ARS, Purdue University and an NSF Grant # 0822495. We thank Janet Shurtleff, Carol Saravitz and the staff of the NCSU phytotron for making this work possible.
- Bent AF, Mackey D: Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Ann Review Phytopath. 2007, 45 (1): 399-436. 10.1146/annurev.phyto.45.062806.094427.View Article
- Hulbert SH, Bennetzen JL: Recombination at the Rp1 locus of maize. Mol Gen Genet. 1991, 226 (3): 377-382.PubMedView Article
- Chintamanani S, Hulbert SH, Johal GS, Balint-Kurti PJ: Identification of a maize locus that modulates the hypersensitive defense response, using mutant-assisted gene identification and characterization. Genetics. 2010, 184 (3): 813-825. 10.1534/genetics.109.111880.PubMedPubMed CentralView Article
- Sun Q, Collins N, Ayliffe M, Smith SM, Drake J, Pryor T, Hulbert S: Recombination between paralogues at the Rp1 rust resistance locus in maize. Genetics. 2001, 158: 423-438.PubMedPubMed Central
- Ramakrishna W, Emberton J, Ogden M, SanMiguel P, Bennetzen JL: Structural analysis of the maize Rp1 complex reveals numerous sites and unexpected mechanisms of local rearrangement. Plant Cell. 2002, 14 (12): 3213-3223. 10.1105/tpc.006338.PubMedPubMed CentralView Article
- Smith SM, Pryor AJ, Hulbert SH: Allelic and haplotypic diversity at the Rp1 rust resistance locus of maize. Genetics. 2004, 167 (4): 1939-1947. 10.1534/genetics.104.029371.PubMedPubMed CentralView Article
- Pryor T: The origin and structure of fungal disease resistance genes in plants. Trends Genet. 1987, 3: 157-161.View Article
- Bennetzen JL, Blevins WE, Ellingboe AH: Cell-Autonomous recognition of the rust pathogen determines Rp1-specified resistance in maize. Science. 1988, 241 (4862): 208-210. 10.1126/science.241.4862.208.PubMedView Article
- Sudupak MA, Bennetzen JL, Hulbert SH: Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. Genetics. 1993, 133 (1): 119-125.PubMedPubMed Central
- Hulbert SH: Structure and evolution of the rp1 complex conferring rust resistance in maize. Ann Rev Phytopath. 1997, 35: 293-310. 10.1146/annurev.phyto.35.1.293.View Article
- Hu G, Richter TE, Hulbert SH, Pryor T: Disease lesion mimicry caused by mutations in the rust resistance gene Rp1. Plant Cell. 1996, 8 (8): 1367-1376.PubMedPubMed CentralView Article
- Smith S, Steinau M, Trick H, Hulbert S: Recombinant Rp1 genes confer necrotic or nonspecific resistance phenotypes. Mol Genet Genomics. 2010, 283 (6): 591-602. 10.1007/s00438-010-0536-5.PubMedView Article
- Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, Hulbert S, Pryor T: Molecular characterization of the maize RP1-D rust resistance haplotype and its mutants. Plant Cell. 1999, 11 (7): 1365-1376.PubMedPubMed CentralView Article
- Chaikam V, Negeri A, Dhawan R, Puchaka B, Ji J, Chintamanani S, Gachomo E, Zillmer A, Doran T, Weil C, et al: Use of mutant-assisted gene identification and characterization (MAGIC) to identify novel genetic loci that modify the maize hypersensitive response. Theor Appl Genet. 2011, 123 (6): 985-997. 10.1007/s00122-011-1641-5.PubMedView Article
- Olukolu BA, Negeri A, Dhawan R, Venkata BP, Sharma P, Garg A, Gachomo E, Marla S, Chu K, Hasan A, et al: A connected set of genes associated with programmed cell death implicated in controlling the hypersensitive response in maize. Genetics. 2013, 193: 609-620. 10.1534/genetics.112.147595.PubMedPubMed CentralView Article
- Balint-Kurti PJ, Johal GS: Use of Mutant-assisted Gene Identification and Characterization (MAGIC) to Identify Useful Alleles for Crop Improvement ISB News Reports 2011. 2011, Blackburg VA, USA: Information Sytems for Biotechnology, 1-3.
- Johal GS, Balint-Kurti P, Weil CF: Mining and harnessing natural variation: a little MAGIC. Crop Sci. 2008, 48 (6): 2066-2073. 10.2135/cropsci2008.03.0150.View Article
- Alcázar R, Parker JE: The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci. 2011, 16 (12): 666-675. 10.1016/j.tplants.2011.09.001.PubMedView Article
- Wang Y, Bao Z, Zhu Y, Hua J: Analysis of temperature modulation of plant defense against biotrophic microbes. Mol Plant Microbe Interact. 2009, 22 (5): 498-506. 10.1094/MPMI-22-5-0498.PubMedView Article
- de Jong CF, Takken FLW, Cai X, de Wit PJGM, Joosten MHAJ: Attenuation of Cf-mediated defense responses at elevated temperatures correlates with a decrease in elicitor-binding sites. Mol Plant Microbe Interact. 2002, 15 (10): 1040-1049. 10.1094/MPMI.2002.15.10.1040.PubMedView Article
- Otsuki Y, Shimomura T, Takebe I: Tobacco mosaic virus multiplication and expression of the N gene in necrotic responding tobacco varieties. Virology. 1972, 50 (1): 45-50. 10.1016/0042-6822(72)90344-3.PubMedView Article
- Dropkin VH: The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology. 1969, 59: 1632-1637.
- Zhu Y, Qian W, Hua J: Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog. 2010, 6 (4): e1000844-10.1371/journal.ppat.1000844.PubMedPubMed CentralView Article
- Chandra-Shekara AC, Gupte M, Navarre D, Raina S, Raina R, Klessig D, Kachroo P: Light-dependent hypersensitive response and resistance signaling against Turnip Crinkle Virus in Arabidopsis. Plant J. 2006, 45 (3): 320-334. 10.1111/j.1365-313X.2005.02618.x.PubMedView Article
- Jr Z, Pink B, Mueller M, Berger S: Light conditions influence specific defence responses in incompatible plantâ€“pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta. 2004, 219 (4): 673-683.
- McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li HH, Sun Q, Flint-Garcia S, Thornsberry J, Acharya C, Bottoms C, et al: Genetic properties of the maize nested association mapping population. Science. 2009, 325 (5941): 737-740. 10.1126/science.1174320.PubMedView Article
- Whitham S, McCormick S, Baker B: The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc Nat Acad Sci. 1996, 93 (16): 8776-8781. 10.1073/pnas.93.16.8776.PubMedPubMed CentralView Article
- Xiao S, Brown S, Patrick E, Brearley C, Turner JG: Enhanced transcription of the Arabidopsis disease resistance genes rpw8.1 and rpw8.2 via a salicylic acid–dependent amplification circuit is required for hypersensitive cell death. Plant Cell. 2003, 15 (1): 33-45. 10.1105/tpc.006940.PubMedPubMed CentralView Article
- Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M, Epple P, Kuhns C, Sureshkumar S, Schwartz C, Lanz C, et al: Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature. 2010, 465 (7298): 632-636. 10.1038/nature09083.PubMedPubMed CentralView Article
- Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J: Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature. 2003, 423 (6935): 74-77. 10.1038/nature01588.PubMedView Article
- Wang W, Barnaby JY, Tada Y, Li H, Tor M, Caldelari D, Lee D-u, Fu X-D, Dong X: Timing of plant immune responses by a central circadian regulator. Nature. 2011, 470 (7332): 110-114. 10.1038/nature09766.PubMedView Article
- Guo A, Reimers PJ, Leach JE: Effect of light on incompatible interactions between Xanthomonas oryzae pv oryzae and rice. Physl Mol Plant Path. 1993, 42 (6): 413-425. 10.1006/pmpp.1993.1031.View Article
- 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 Phys. 1999, 119 (4): 1233-1242. 10.1104/pp.119.4.1233.View Article
- 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 (6): 941-954. 10.1111/j.1365-313X.2007.03191.x.PubMedView Article
- Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J: A Kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science. 2009, 323 (5919): 1357-1360. 10.1126/science.1166289.PubMedView Article
- Holland JB, Nyquist WE, Cervantes-Martínez CT: Estimating and interpreting heritability for plant breeding: an update. Plant breed Rev. 2003, 22: 9-112.
- Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F: Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Bio. 2006, 62 (1): 305-323.View Article
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.