Disease Lesion Mimic Mutants of Maize
Gurmukh S. Johal
Department of Botany and Plant Pathology
Purdue University
West Lafayette, IN 47907
Ph: 765-494-4448
(Corresponding author: gjohal@purdue.edu)
Introduction
Disease lesion mimics are a class of mutants in plants that spontaneously form lesions
(patches of dead cells) in the absence of any obvious injury, stress or infection to the plant.
Initially, these mutants were thought to have resulted solely from defects in genes and
pathways that are normally called into action during the infectious encounters of plants with
pathogens, and were therefore named disease lesion mimics (27,34). While this is true with
some of these mutants, recent studies have demonstrated that the "disease" underlying
disease lesion mimic mutants encompasses much more than simply mimicking plant
responses to pathogens. As described in detail later, these lesioned mutants (abbreviated
les or Les for recessive and dominant mutants, respectively) result from aberrations in all
sorts of biological processes, with loss of cellular homeostasis (stable equilibrium within the
cell) a common feature that eventually results in the death of affected cells (7,17,22).
The Repertoire of Maize Les/les Mutants
Lesion mimic (Les/les) mutants are present ubiquitously in plants. In Arabidopsis, they
have been described by many names, including lesions simulating disease (lsd) or
accelerated cell death (acd) mutants (7,22), and in rice they are called spotted leaf (spl)
mutants (35,36). In maize (Zea maydis), where lesion mimics were isolated first, more than
50 loci (positions in a chromosome) have been identified that give rise to a lesioned
phenotype when aberrant (4,17,34). Intriguingly, more than half of these mimics inherit in
a partially or completely dominant fashion, making them the largest class of gain-of-function
mutations in maize.
Almost every Les/les mutant is unique in some aspect and produces different symptoms
on affected plants. The phenotypes vary, with lesions ranging in number from a few to many,
in size from minute flecks to lesions that cover the whole leaf, and in color from dark brown
to chlorotic or even translucent (Figs. 1 through 5). In shape, lesions of most Les/les mutants
are more or less circular, but there is at least one mutant (les*-2014) in which lesions form
along the length of the leaf (Fig. 6). In most Les/les mutants, lesions are confined to the leaf
blade, but a few mutants also form lesions on the leaf sheath and stalk (Fig. 7), causing the
plants to lodge or collapse prematurely.
Fig. 1. Initiation and expansion of Les6 lesions.
Fig. 2. Les9 lesions appear as water soaked spots
immediately following their initiation. Later these lesions
turn yellowish brown as shown in Fig. 10.
Fig. 3. Highly concentric and expanding lesions of lls1
Fig. 4. Typical chlorotic lesions underlying Les39.
that engulf the entire leaf.
Fig. 5. Translucent lesions of les54, which was
Fig. 6. Long and narrow lesions of les*-2014. Initially the
previously called clear-spotted mutant.
lesions appear as water soaked streaks that collapse
within a day or two to exhibit the typical dried-up
appearance.
Depending on how lesions behave
Fig. 7. Typical Les4
lesions that form not only on
leaf blades but also on the
leaf sheath, husks and
eventually on lower stalk
internodes, causing the
plant to break.
following inception (initiation), Les/les
mutants can be divided into two general
categories: determinative and
propagative (7,17). In determinative
mimics, lesions are often initiated
profusely but then are restricted in size,
giving the illusion of a massive
hypersensitive response (HR), a kind of
suicidal reaction of plant cells triggered in
response to invasion by incompatible
pathogens (7). In contrast, propagative mimics form lesions relatively sparingly, but once
formed lesions often expand uncontrollably to kill the entire leaf and even the entire plant
(7,22). It is presumed that lesions in the determinative mimics class arise from impairments
that result in the lowering of the threshold for cell death initiation. In comparison,
propagative mimics are thought to represent defects in genes that encode negative
regulators of cell death in plants. It should be emphasized, however, that not all mutants fall
cleanly into these two categories; there are a number of mutants that initially cause discrete
lesions but ultimately cause the affected leaves to senesce and collapse much earlier than
the corresponding leaves on wild-type siblings.
Factors Affecting Les/les Mutants
Although Les/les mutants are strictly Mendelian mutants, their phenotype is easily
influenced by a number of other factors, both external (environmental) and internal (host
factors), causing many lesion mimic mutants to behave as conditional mutants.
Environmental factors
· Light. Among the environmental factors, light appears to be most important in
mediating lesion formation. A vast majority of the maize mimic mutants require light for
the initiation and/or propagation of lesions (4,15,17). The effect of light on Les/les
mutants can be easily revealed by covering a part of the leaf with aluminum foil or some
dark paper that prevents light from reaching the leaf (11,15,31). Alternatively, light
effect can be shown by introgressing Les/les into other mutant backgrounds that are
deficient in chlorophyll accumulation and/or some other aspect of photosynthesis.
Experiments with such double mutants have demonstrated that it is the incident light
that is important for lesion initiation and/or propagation for certain Les/les mutants
(15), but it is the light harvested for photosynthesis that fuels lesion formation in other
mutants (11).
· Temperature. Temperature also plays an important role in the initiation of lesions
accompanying many mimics. In some cases, there may be a strict requirement of
temperature [for instance, the phenotype of Les1 only manifests optimally at
temperatures below 60°F (13)], but, in general, most Les/les mutants exhibit a severe
phenotype when the temperature is high and the light is bright (17).
· Glasshouse vs. field-grown plants. Finally, the
overall growing conditions, especially whether the
plants are growing in a glasshouse or in the field, also
have a major impact on the severity of Les/les
mutants. Intriguingly, compared to field conditions,
phenotypes of some of these mutants are enhanced
under greenhouse conditions, while phenotypes of
others are suppressed (Johal, unpublished data).
These observations suggest complex interactions
between Les/les mutants and environmental factors.
Fig. 8. Typical progression of a Les/les
phenotype as the plant develops. The
mutant shown here is Les17.
Host factors
· Developmental factors. Almost all maize Les/les
mutants are programmed to manifest their
phenotype in a developmentally specified fashion. While some of them are expressed
around the time of flowering (Les4, for example) or later, a vast majority of them begin
expression about 3-4 weeks after planting. In the latter case, lesions first appear as tiny
spots near the tip of the first leaf of field-grown mutant plants, about 4-weeks after
emergence. These lesions enlarge in size while new ones emerge down the leaf blade
following a basipetal gradient. This results in the entire leaf being covered with lesions
in 4-5 days. Meanwhile, lesions have already started to develop near the tip of the
second leaf (Fig. 8). This pattern continues until the plant is fully covered with lesions,
shortly around pollen shed (10,31). What dictates this developmental behavior of
Les/les mutants remains unknown.
Genetic background factors. It is well known that the penetrance (whether or not a given
phenotype is detected) and expressivity (phenotypic severity) of Mendelian mutants are
easily influenced by the genome (the genetic background) in which they reside. Nowhere is
it more dramatic than with the maize Les/les mutants which may have a lethal phenotype in
one genetic background but a benign one in another (29). A number of maize inbred lines
have been identified that markedly dampen or exacerbate symptoms associated with many
of the lesion mimic mutants. For example, the inbred Mo20W, which remains green for
prolonged periods after fertilization, tends to suppress
·many Les/les mutants when introgressed into its genome (10,29,31). In contrast, many
of these mimics express so severely in the inbred W23 background that the mutant
plant either dies before reaching maturity or fails to produce seed (29).
The dramatic nature of the genetic background effect on maize lesion mimics was first
demonstrated by Neuffer, who was also the first one to unveil Les/les mutants as a unique
phenomenon in plants (13,29). Employing simple genetic crosses involving inbred Mo20W
and Les1 in the inbred W23 background (Les1::W23), it was found that the suppressible
effect of Mo20W on Les1 was dominant over its optimal expression in W23. When F2
populations of this cross were evaluated, a range of mutant phenotypes, with varying
degrees of severity, were found segregating in the progeny, indicating the involvement of
multiple genetic factors in shaping the phenotype of Les1.
One intriguing implication of this study was that the exquisite sensitivity of the Les/les
phenotype to a maize genetic background could be used as an indicator or reporter to
delineate the nature of this poorly-understood but ever-present genomic variable in maize.
We addressed this possibility by taking advantage of les23, a recessive loss-of-function
mutant, and a QTL (quantitative trait locus) approach, which was based on an F2 population
derived from a cross between les23 and Mo20W (31). This study led us to identify a strong
QTL that was able to contribute to more than 70% of the variation in les23 phenotypes
present in this population. This QTL, which we have named Slm1 (suppressor of lesion
mimics-1), has been mapped to the long arm of chromosome 2 in maize. A few minor QTL
were also identified that together with Slm1 completely suppress les23 (31). Similar studies
with Rp1-D21, a partially dominant Les mutant resulting from an aberration in the maize Rp1
disease resistance gene, have uncovered additional suppressors like Slm1 (Johal,
Balint-Kurti et al., unpublished data).
In fact, so common are these suppressors in the maize germplasm that they can also
cause a lesion mimic mutant to become cryptic. A case in point is inbred Mo17 whose hybrid
with B73 was used commercially in the 1960s and 1970s. Using IBM RILs (IBM = intermated
B73 and M017; RIL = recombinant inbred lines) between these two lines as well as
segregating F2 populations of Mo17 with B73 and four other inbred lines, we were able to
reveal a les locus in Mo17, which we have named les-Mo17 (Penning, Johal et al.,
unpublished data). However, les-Mo17 is prevented from manifesting a phenotype in Mo17
because of the presence of two unlinked suppressors in this inbred. However, when these
suppressors segregate away from les-Mo17 (as accomplished in the IBM RILs or F2
populations), les-Mo17 reveals itself by expressing a les phenotype.
Les/les Effect on Maize Diseases
It has been well documented in Arabidopsis that Les/les mutants often enhance the ability
of plants to resist diseases, especially those that are caused by pathogens using biotrophic
lifestyles for invasion (22). Similar observations have been made in rice in which many of the
Spl/spl mutants induce systemic acquired resistance (SAR) to the rice blast pathogen
(Magnaporthe grisea) (35,36). This, however, does not seem to be the case in maize. With
the exception of Rp1-derived Les/les mutant causing broad spectrum resistance against the
rust pathogen Puccinia sorghi (14), most maize Les/les mutants have not been found to
induce effective SAR to any of the pathogens that have been studied in detail. This includes
the leaf spot pathogen Cochliobolus carbonum, a necrotroph, and the common rust pathogen
P. sorghi, an obligate biotroph. Instead of the pathogen being suppressed, P. sorghi has been
found to suppress lesions associated with a few Les/les mutants (Fig. 9). While SAR has not
been observed to be induced by maize Les/les mutants, local induction of resistance has
been seen in some cases. A dramatic example of this is provided by Les9 which suppresses
largely the symptoms associated with the gray leaf spot disease caused by Cercospora
zea-maydis (Fig. 10). Why maize Les/les mutants differ from other plants with regard to
their ability to induce SAR is unknown.
Fig. 9. Cell death underlying Les29 lesions is
Fig. 10. Leaves of two sibling plants carrying or lacking
suppressed in the vicinity of common rust pustules,
the Les9 mutation. While the wild-type leaves (bottom)
thereby producing areas of protected leaf tissue that
were inundated by infection by the gray leaf spot
plant pathologists often refer to as 'green islands.'
pathogen (C. zea-maydis), Les9 leaves (top) exhibited a
high level of resistance to the pathogen.
Why Study Lesion Mimics?
Lesion mimic mutants exhibit two key features that have aroused much interest in their
investigation. First, as mentioned earlier, they often exhibit induction of defense responses
which are typically upregulated at the time of pathogen infection (7,17,22). This association
has led many researchers to believe that lesion mimic mutants represent a valuable resource
for studying the intricacies of plant defense without having to worry about the compounding
effects from pathogens.
The second feature is the ubiquitous association of these mimics with cell death, which
either happens precociously in these mutants or is not contained adequately following
normal onset. As a result, ideas have been elaborated to suggest that Les/les mutants
represent defects in genes and mechanisms that control the programmed death of cells and
tissues in plants (7,17). Programmed cell death (PCD) is as important in plants as it is in
animals; it serves many essential roles in the growth and development of plants, as well as
in their defense against biotic and abiotic stresses (7,19). Despite the importance of PCD, our
knowledge of how plants regulate and accomplish PCD remains rudimentary.
In contrast, great advances have been made in animals over the last decade to show that
the cellular machinery of PCD, also called apoptosis, are largely conserved from worms to
humans (32). For instance, cells that are fated to die apoptotically shrink and their cell and
nuclear membranes undergo blebbing (formation of irregular bulges in membranes). This is
followed by breakage and packaging of cellular contents into vesicles called apoptotic bodies,
which are phagocytosed (consumed) by neighboring cells. Meanwhile, the nuclear DNA of
dying cells is degraded, first into high molecular weight DNA and subsequently into
oligonucleosomal ladders. Such apoptotic dismantling of the cell is brought about by a class
of cysteine proteases termed caspases. Produced as zymogens (inactive enzyme precursors),
the processing, activation and function of caspases is controlled by the opposing action of an
ever-increasing number of cell death suppressors and enhancers. Mitochondria play a central
role in this battle of pro-death versus anti-death factors. Their integrity is breached when
pro-death factors outcompete the anti-death factors, causing mitochondria to release a slew
of molecules (including cytochrome C) that then activate caspases (2,6,32).
Although some progress has been made recently in plant PCD (12,20), no such
framework of genes and mechanisms has yet emerged that may underlie PCD in plants. So
it is hoped that an exploration of the Les/les phenomenon will fill this void and provide
valuable information concerning how cell death is signaled, controlled, and executed in
plants. Given what the recent cloning and subsequent characterization of a number of lesion
mimic genes from Arabidopsis, maize, barley, rice and tomato have revealed (4,22), there
are ample reasons to be excited about this possibility.
Why So Many Mimics?
The Les/les phenotype has emerged as one of the most common mutant phenotypes in
plants. As mentioned earlier, more than 50 Les/les loci have been identified in maize, and
judging from the rate at which new lesion mimic mutations are being identified in Arabidopsis,
a similar number may soon be approaching in this dicot model as well. In maize, Les/les loci
have been found to scatter all over the genome (28), and only a few of them exist as multiple
mutant alleles. Extrapolating from this general lack of confirmed allelic pairs, it has been
suggested that more than 200 Les/les loci might exist in maize (34).
The question arises: why are there so many mimic mutation loci in plants? The recent
cloning and characterization of a number of lesion mimic genes have provided significant
insights into this question [reviewed in (4,22)]. It appears that lesion mimic mutations can
result from a variety of mechanisms, some of which include:
· Genetic aberrations in plant R genes (disease resistant genes) (14,33,37). A key
example is that of the maize Rp1 gene that confers resistance to the common rust
pathogen Puccinia sorghi. As mentioned earlier, alleles of this gene have been identified
that trigger hypersensitive cell death response (HR) spontaneously. These alleles have
undergone simple changes in their structure that result in autoactivation of the RP1
protein, which, like other R genes, is normally kept in check by both intra- and
intermolecular interactions.
· Defects in genes downstream of R genes. A classic example of this is the tomato nec1
gene which is required for proper functioning of the Cf2 disease resistance gene (9,18).
· Defects in genes that may work at the interface of PCD and defense signaling (5,35).
The mlo mutant of barley is a case in point. It is defective in a seven membrane protein
that modulates resistance at the level of cell wall and cell death. A recent example of
this is the rice Spl11 gene which is defective in an E3 ligase (36).
· Mutations in genes involved in reactive oxygen intermediates (ROI) accumulation and
management (8,25). Excessive production and/or excessive accumulation of ROI is
probably the most common mechanism underlying the etiology of Les/les mutants. This
happens in the case of the Arabidopsis lsd1 mutant which is defective in a zinc-finger
protein. The phenotypes of the Arabidopsis acd2 and maize lls1 mutants, which have
defects in chlorophyll degradation, result from light-dependent production of singlet
oxygen (10,24). The maize Les22 mutant, which is defective in chlorophyll biosynthesis
(15), also owes its lesion mimic phenotype to singlet oxygen.
· Defects in cell death pathway(s) mediated by ceramides, a family of lipid molecules
composed of sphingosine and a fatty acid, and found in high concentrations in cell
membranes (3,21,23). This is exemplified by the acd5 and acd11 genes of Arabidopsis,
which have lesions in a ceramide kinase and sphingosine transfer protein, respectively
(3,21).
· Errors or impairments in metabolism (15). The maize mutant Les22, which is defective
in a single copy of the gene Urod that encodes an enzyme of tetrapyrrole biosynthesis
(15), is a key example of this. The maize lls1 and the Arabidopsis acd2, which encode
pheophorbide oxidase and RCC reductase (two consecutive enzymes of the chlorophyll
degradation pathway) exemplify another set of mutants belonging to this class (10,24).
· Errors in various membrane associated functions (1,16). These defects are highlighted
by the Arabidopsis ssi2, (defective in a plastidic stearoyl-acyl-carrier protein
desaturase), acd6 (defective in ankyrin-repeat domain containing transmembrane
protein), hlm1 (defective in a cyclic nucleotide gated ion channel), cpn1 (defective in
calcium-dependent, phospholipids binding proteins called copines), cpr5 (defective in a
novel five transmembrane domain protein), and nsl1 (defective in a membrane attack
complex/perforin domain containing protein (reviewed in 22).
· Aberrations in vesicle mediated transport. A classic case of this is the barley mlo mutant
which is defective in a serpentine membrane protein, a regulator of wall based
penetration resistance to fungal pathogens of the powdery mildew class. MLO appears
to do so by regulating the functioning of various SNARE proteins (soluble
N-ethylmaleimide sensitive fusion protein attachment receptors) (30). We have also
unveiled a similar lesion mimic mutant in maize. The rust mimic-1 mutant is defective
in a SNAP-25 (synaptosome-associated protein of 25,000 daltons) homologue and as a
result results in light-dependent lesion mimicry (Johal et al., unpublished data)
In addition, the lesion mimic phenotype has also been found to be readily induced by a
variety of transgenes, including those that normally perform house-keeping functions in cells
[reviewed in (26)], suggesting that whenever things get out of sync (general loss of
homeostasis), plant cells are tripped to embrace pathways leading eventually to their
demise.
Conclusion
The Les/les phenotype is emerging as one of the most common stress phenotypes in
plants. These mutants encompass much more than simply mimicking plant responses to
pathogens. One useful aspect of the Les/les phenotype is that it can be discerned and
quantified rather easily, making it an excellent indicator (reporter) of stress in plants. Les/les
mutants thus provide a unique opportunity to look into genes and pathways that enhance or
suppress the extent of stress associated with these mutants. A better understanding of the
biology of Les/les mutants and the genes and mechanisms that impact their etiology holds
promise for generating crops capable of withstanding all sorts of stresses that plants have to
face in an ever-changing environment.
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