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First published online 13 August 2008
doi: 10.1242/dev.024273
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Research Report |
1 Plant Gene Expression Center, United States Department of Agriculture -
Agriculture Research Service and the University of California, Albany, CA
94710, USA.
2 Pioneer - A DuPont Company, Johnston, IA 50131, USA.
* Author for correspondence (e-mail: gchuck{at}nature.berkeley.edu)
Accepted 9 July 2008
SUMMARY
Grass flowers are organized on small branches known as spikelets. In maize, the spikelet meristem is determinate, producing one floral meristem and then converting into a second floral meristem. The APETALA2 (AP2)-like gene indeterminate spikelet1 (ids1) is required for the timely conversion of the spikelet meristem into the floral meristem. Ectopic expression of ids1 in the tassel, resulting from a failure of regulation by the tasselseed4 microRNA, causes feminization and the formation of extra floral meristems. Here we show that ids1 and the related gene, sister of indeterminate spikelet1 (sid1), play multiple roles in inflorescence architecture in maize. Both genes are needed for branching of the inflorescence meristem, to initiate floral meristems and to control spikelet meristem determinacy. We show that reducing the levels of ids1 and sid1 fully suppresses the tasselseed4 phenotype, suggesting that these genes are major targets of this microRNA. Finally, sid1 and ids1 repress AGAMOUS-like MADS-box transcription factors within the lateral organs of the spikelet, similar to the function of AP2 in Arabidopsis, where it is required for floral organ fate. Thus, although the targets of the AP2 genes are conserved between maize and Arabidopsis, the genes themselves have adopted novel meristem functions in monocots.
Key words: AP2, Maize, Meristem, miR172
INTRODUCTION
Meristems provide cells for all the tissues and organs of the plant, and
understanding their activity is essential to decipher the evolution of plant
architecture (Sussex and Kerk,
2001
). Meristems can be classified as determinate or indeterminate
based on whether they terminate in the production of primordia. Inflorescence
meristems (IMs), such as those of racemes, are usually indeterminate,
producing an open number of lateral meristems. Floral meristems (FMs), by
contrast, are usually determinate and terminate in the production of floral
organs. The switch from indeterminacy to determinacy may also be considered in
the light of developmental timing, or heterochrony. For example, if a switch
to determinacy is delayed, the meristem will initiate extra lateral organs
before terminating.
Inflorescence architecture in monocots is dependent upon the initiation of
specific meristem types (McSteen et al.,
2000). In maize, several lateral meristems with defined branching
activity are initiated before FMs are made. These include branch meristems
(BMs), spikelet pair meristems (SPMs) and spikelet meristems (SMs). Spikelets,
the fundamental floral unit of all monocots
(Clifford, 1987), consist of
two bract leaves, called glumes, that enclose a variable number of florets.
Maize SPM and SM are determinate. The SPM produces one SM and then terminates
its activity by differentiating into an SM. Similarly, the SM produces one FM
and then terminates by becoming an FM.
Several maize and rice mutants have provided clues as to how meristem fates
are acquired. SM identity is controlled by the action of the orthologous genes
branched silkless1 (bd1) in maize
(Chuck et al., 2002) and
frizzy panicle1 (fzp1) in rice
(Komatsu et al., 2003). In
bd1 and fzp1 mutants, the spikelet meristem is replaced by
an indeterminate branch meristem. The bd1 and fzp1 genes
encode members of the ERF family of APETALA2 (AP2) transcription factors, and
function to repress indeterminate lateral branch meristem fates. SM
determinacy is controlled by another AP2 transcription factor, encoded by the
indeterminate spikelet1 (ids1) gene
(Chuck et al., 1998).
ids1 mutant spikelets are indeterminate and initiate extra florets
instead of two. In rice, a similar phenotype is seen in the supernumerary
bract (snb) mutant, which delays the floral transition and
produces extra glumes before initiating florets. snb encodes an AP2
transcription factor similar to ids1, and might represent a
paralogous gene (Lee et al.,
2006). ids1 is targeted by the MIR172 microRNA
encoded by the tasselseed4 (ts4) gene
(Chuck et al., 2007).
Mutations within the microRNA binding site of ids1 give rise to the
dominant Tasselseed6 (Ts6) allele, which affects spikelet
meristem branching and sex determination of floral organs
(Chuck et al., 2007). Double
mutant analysis has shown that ids1 mutants suppress the ability of
the ts4 SM to initiate ectopic FMs. Thus, ids1 has diverse
functions, affecting sex determination as well as meristem determinacy.
The orthologous floral homeotic genes LEAFY (LFY) of
Arabidopsis and FLORICAULA (FLO) of
Antirrhinum play major roles in the specification of FM identity in
these diverse species (Weigel et al.,
1992; Coen et al.,
1990). Flowers on lfy mutants have characteristics of
both floral and inflorescence meristems
(Schultz and Haughn, 1991;
Huala and Sussex, 1992;
Weigel et al., 1992), whereas
flowers on flo mutants are complete transformations to
inflorescences. LFY activates expression of the MADS-box genes
APETALA3 (Lamb et al.,
2002) and AGAMOUS
(Hong et al., 2003), both of
which function in specifying floral organ identity. Mutations in the maize
LFY/FLO orthologs, zfl1 and zfl2, affect floral
organs and tassel branch number (Bomblies
et al., 2003). Knock-down of the rice LFY/FLO ortholog,
RFL, affects flowering time and panicle branching, yet spikelets and
florets are still made (Rao et al.,
2008).
Here we describe a paralog of ids1, sister of indeterminate spikelet1 (sid1), in maize. sid1 functions together with ids1 to specify the fate of several lateral meristems in the inflorescence. Fewer branches form in the tassel and fewer rows of spikelet pairs form in the ear. Both ear and tassel spikelet meristems are indeterminate and produce supernumerary organs. The tassel spikelets reiteratively produce bracts and never produce sex organs. The spikelets in the ear also produce many bracts, but eventually terminate in an ovule-like structure. Late-forming bracts in the ear are feminized owing to the ectopic expression of AGAMOUS-like genes in maize. Thus, ids1 and sid1 are needed to promote determinacy and produce sex organs, similar to LFY/FLO function in Arabidopsis and Antirrhinum.
MATERIALS AND METHODS
Phylogenetic analysis
Phylogenetic analysis was performed using MrBayes v. 3.1.2
(Ronquist and Huelsenbeck,
2003) Markov chain Monte Carlo (MCMC) algorithm using the
Time-Reversible model (GTR) with a proportion of invariable sites (I) and a
gamma distribution parameter (G). The analysis was run for 10,000 generations,
sampling trees every 10 generations; 250 trees were discarded as burn in. Tree
shows average branch lengths and posterior probabilities for all resolved
nodes.
Expression analysis
Poly(A)+ RNA gel blots and in situ hybridization were performed
as described (Chuck et al.,
2007). For sid1 in situ hybridizations, a 3'
fragment outside the AP2 domain and including the 3' UTR (bp 1301-1730)
was used. This same fragment was used to probe northern blots. Probes for
kn1 (Jackson et al.,
1994), bd1 (Chuck et
al., 2002) and zag1
(Schmidt et al., 1993) were
used as previously described.
Cleavage assay
Poly(A)+ RNA (200 ng) was isolated from 0.5 cm ear primordia
from B73 and ts4-TP and used directly for ligation to the GeneRacer
5'-RACE oligo (Invitrogen) and reverse transcribed. One microliter of
the reverse transcription reaction was used for RT-PCR using the GeneRacer
5'-RACE oligo in combination with the SID1 53R oligo
(5'-AACCATACCCAACAGTGGCGACTG-3') located 280 bases from the
microRNA binding site. The wild-type cleavage product was cloned into pGEM-T
Easy (Promega) and sequenced using M13 primers.
Double mutants
Double mutants between ids1-mum1 and sid1-mum4, between
ids1-Burr and sid1-mum3, and between ids1-mum1,
sid1-mum1 and ts4-A were made by selfing heterozygotes.
Homozygotes for sid1 were scored by PCR using sid1 oligos
607 and 608 (5'-ATCAGCGTGTGCCTAGCATTTCTTCCCT-3' and
5'-CAGTCCCTGCACAATTGGACGACACA-3'). ids1 homozygotes were
scored using ids1 oligos 804 and 674
(5'-ATCGCAGCTCGATCGTATG-3' and
5'-TACAGGGGCGTCACCTTCTA-3'). ts4-A homozygotes were
scored using ts4 oligos 7F and 7R
(Chuck et al., 2007).
RESULTS AND DISCUSSION
sid1 is targeted by miR172
Previous work identified five potential MIR172 targets
(Chuck et al., 2007).
AY109248.1, now referred to as sid1, had high sequence similarity to
ids1, especially within the AP2 domain, where it displayed 96% amino
acid identity (Fig. 1A). A
Bayesian phylogenetic tree of MIR172 targets in rice and maize showed
that sid1 shares a common ancestor with ids1
(Fig. 1B), and is likely to be
orthologous to the rice snb gene, which controls the SM-to-FM
transition (Lee et al., 2006).
To determine the function of sid1, Mutator (Mu) transposons
were employed to generate loss-of-function alleles
(Bensen et al., 1995). Four
Mu insertions were isolated in sid1, three in exons and one
in an intron (Fig. 1C).
sid1-mum1 and sid1-mum2 alleles had no transcript, whereas
the sid1-mum3 and sid1-mum4 alleles had longer transcripts,
possibly owing to alternative splicing of the Mu element
(Fig. 1F).
A combination of RT-PCR and RNA gel blots was performed to determine
sid1 transcript levels in the wild type and in ts4 and
ids1 mutants. RT-PCR demonstrated that sid1 is widely
expressed in all tissues assayed, including roots, leaves and inflorescences,
and is elevated in tassels from ts4 mutants
(Fig. 1D). An increase in
sid1 transcript levels was also detected by gel blots with RNA from
ts4 mutant tassels (Fig.
1F) and ears (Fig.
1G), indicating that the sid1 transcript might be subject
to negative regulation by ts4. In support of this, RNA cleavage
assays of sid1 transcripts from ts4-TP mutants, as compared
with those from wild type, showed differences in the amount of cleavage within
the microRNA binding site. In ts4-TP mutants, most transcripts were
cleaved 3' of the microRNA binding site
(Fig. 1E). By contrast, in
wild-type RNA, almost all transcripts were cleaved between bp 10 and 11 of the
microRNA binding site, as expected. Some cleavage of sid1 still
occurred in ts4-TP within the microRNA binding site, suggesting that
sid1 is also targeted by other members of the MIR172 family,
of which there are at least four (Chuck et
al., 2007). sid1 expression was also increased in
ids1 mutant ears as compared with wild type
(Fig. 1G). This finding
indicates that sid1 might be under negative regulation by ids1.
AP2 genes are predicted to be negatively autoregulated in both
Arabidopsis (Schwab et al.,
2005) and wheat (Simons et
al., 2006). Compensation between redundant genes has been
documented in numerous cases, for example with the PIN genes in
Arabidopsis. Mutations in pin7 result in ectopic expression
of PIN4, and PIN1 is ectopically induced in pin2
mutants (Vieten et al.,
2005).
The function of ids1 and sid1 in spikelet meristem fate
Maize is a monoecious plant, in which male and female flowers are borne on
distinct inflorescences. Sex determination occurs through abortion of carpel
primordia in the tassel and arrest of stamen primordia in the ear
(Cheng et al., 1983). Ears and
tassels also differ by the presence of BMs, which form side branches in the
tassel and are absent from the ear (Fig.
2A, Fig. 3A). SPMs
initiate in ordered rows in a spiral phyllotaxy from the inflorescence
meristem and in a distichous phyllotaxy along the tassel branches
(Fig. 3A,B). Each SPM initiates
an SM and converts to a second SM. Each SM initiates two sterile leaves called
glumes, followed by two lemmas, each containing FMs in their axils. The FM
initiates a palea, lodicules, stamens and finally a pistil, or silk
(Fig. 3C,D). In tassels, the
pistils abort to produce a pair of staminate florets
(Fig. 2H), whereas in the ear,
the lower floret and the stamens abort to produce a single pistillate floret
(Fig. 2D)
(Cheng et al., 1983).
Since sid1 mutants appeared to be phenotypically normal (data not
shown), double mutants with ids1 were analyzed. These double mutants
affected all the lateral meristems of the inflorescence. The tassels of the
ids1-Burr;sid1-mum3 double mutant
(Fig. 2A) had fewer branches
than with ids1-Burr alone
(Kaplinsky and Freeling,
2003). Normal female inflorescences initiate seven to eight rows
of SPMs, but ids1-Burr;sid1-mum3 double mutants initiated a maximum
of four rows, and often had bare rachis in place of the missing rows
(Fig. 2B). Although the ears of
the double mutant appeared to initiate silks, seed set was reduced 5- to
8-fold compared with ids1-Burr
(Fig. 2C), indicating that
floral organ function was affected. In fact, most of the seeds that formed
failed to germinate. ids1-Burr ear spikelets initiate extra lateral
florets in the axils of lemmas (Fig.
2E). In the double mutant, these extra lateral florets were
absent, and the spikelet terminated in a floret-like structure
(Fig. 2F,G). This terminal
structure was enclosed by several bracts that have silk-like characteristics
at their tips (Fig. 2G).
ids1-Burr tassel spikelets also initiate several functional florets
(Fig. 2I). The tassels of the
double mutant, however, did not initiate any florets, and continuously
initiated bracts instead (Fig.
2J). A double mutant between different alleles, ids1-mum1
and sid1-mum4, appeared identical to ids1-Burr;sid1-mum3
(data not shown), and thus these phenotypes are not allele-specific.
|
). Thus, at
least one other target gene must be responsible for the continued presence of
the ts4 ear phenotype in the ids1;ts4 double mutant. Double
mutants between sid1-mum1 and ts4-A resembled ts4-A
alone in both the tassel (Fig.
2L) and ear (Fig.
2N, left). However, when these double mutants were also made
heterozygous for ids1-mum1, the tassel was normalized and resembled a
weak ts4 mutant phenotype (Fig.
2M), whereas the ear resembled that of wild type
(Fig. 2N, right). This result
supports the RNA analysis (Fig.
1D,F,G) and indicates that sid1 is a ts4 target
gene, although its suppressive effects can only be observed in combination
with ids1. The ids1-mum1;sid1-mum1;ts4-A triple mutant
resembled the ids1-Burr;sid1-mum3 double mutant and completely
suppressed the ts4 sex-determination phenotype in the tassel
(Fig. 2A, right) and extra
branching phenotypes in the ear (data not shown). Thus, ids1 and
sid1 together are epistatic to ts4. Scanning electron microscopy was used to examine the ids1;sid1 double mutant phenotype more closely. ids1-mum1 ear tips normally initiate six rows of spikelet pair meristems (Fig. 3E). ids1-mum1 ear spikelets normally initiate several extra lemmas, each of which contains FMs in their axils (Fig. 3F). These extra FMs are fully functional, and initiate floral organs in a normal pattern (Fig. 3G). By contrast, ids1-Burr;sid1-mum3 tassels initiated fewer BMs (Fig. 3H), and only four rows of SPM (Fig. 3I). The SM of the tassel in the double mutant was indeterminate and continuously initiated lemma-like bracts with no FMs (Fig. 3J). The ear of the double mutant also initiated fewer rows (Fig. 3K, Fig. 4G). In contrast to the tassel, the SM of the ear terminated in an ovule-like structure after initiating several bracts (Fig. 3L). No stamens or lodicules were observed, indicating that the normal pattern of floral organ initiation is not followed in the double mutant. Later in development, the tips of the bracts began to differentiate structures that resemble silks (Fig. 3M).
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Expression patterns of meristem markers suggest that the SM never transitions to FM fate in ids1;sid1 mutants
In situ hybridization using meristem-specific markers was carried out to
further understand the basis for the indeterminacy and organ identity defects
in ids1;sid1 double mutants. The maize knotted1
(kn1) gene is expressed in the indeterminate cells of the meristem
and is downregulated upon organ initiation
(Jackson et al., 1994).
Cross-sections of ids1-Burr ears compared with
ids1-Burr;sid1-mum3 ears showed that the number of rows of SPMs was
reduced (Fig. 4, compare F with
G). kn1 expression in the spikelets of the double mutant persisted
after the initiation of several sterile bracts
(Fig. 4H), indicating that the
meristem is indeterminate. The branched silkless1 (bd1) gene
is expressed in a semi-circular domain at the base of the SM and disappears
upon floret initiation in maize and rice
(Chuck et al., 2002). In young
ids1-Burr;sid1-mum3 spikelets, the bd1 expression pattern
appeared normal (Fig. 4I).
Later in development, however, instead of disappearing, this expression
pattern persisted (Fig. 4J),
demonstrating that the meristem had retained SM identity longer than
normal.
The maize AGAMOUS-like MADS-box genes zmm2 and
zag1 are duplicate genes that mark the FM as well as stamens and
carpels (Schmidt et al., 1993;
Mena et al., 1996)
(Fig. 4K,M). They are not
expressed in leaf-like organs, such as palea or lemma. zag1 mutations
cause extra carpels to form that fail to fuse into a functional silk
(Mena et al., 1996). At early
stages of spikelet development, we saw no expression of zmm2 (data
not shown) or zag1 (Fig.
4N, inset) in the ids1;sid1 double mutant. However,
ectopic zmm2 expression was observed later in the SM of the double
mutant as well as in the carpelloid bracts near the apex
(Fig. 4L). zag1 was
ectopically expressed in these same regions
(Fig. 4N). The ectopic
expression of AGAMOUS-like MADS-box genes in the ids1;sid1
double mutant is consistent with the role of the Arabidopsis AP2 gene
as a negative regulator of AGAMOUS
(Drews et al., 1991). Finally,
the maize AP3 ortholog, silky1, which is necessary for
stamen and lodicule patterning (Ambrose et
al., 2000), was not expressed in the double mutant at early (not
shown) or late (Fig. 4P)
stages, whereas it was detected in the stamens or lodicules of wild-type
controls (Fig. 4O).
Based on previously described differences between the ts4 and
Ts6 mutant phenotypes (Chuck et
al., 2007), it was postulated that at least one other gene was
targeted by the ts4 microRNA in addition to ids1. sid1
appears to be that gene based on four criteria: its expression levels are
elevated in ts4 mutants (Fig.
1D,F,G); its cleavage is reduced in a ts4 mutant
background (Fig. 1E); it is
ectopically expressed in ts4 mutant inflorescences
(Fig. 4E); and sid1
mutants enhance suppression of the ts4 mutant phenotype by
ids1-mum1 (Fig. 2N).
Previous work showed that MIR172 represses its AP2 target
genes at the level of translation (Chen,
2004; Aukerman and Sakai,
2003). Other groups have found that MIR172 repression may
act at both the level of translation and transcript cleavage
(Schwab et al., 2005). We
showed that IDS1 is regulated at the level of translation by ts4
(Chuck et al., 2007). Our
analysis of sid1 suggests that it is regulated at the level of
transcript stability, although we cannot rule out an additional level of
translational regulation. Thus, it is likely that ts4 regulates
AP2 transcripts using both modes of regulation.
|
;
Chuck et al., 2007).
Surprisingly, ids1 mutants also initiate extra florets, but in a
defined distichous phyllotaxy. Thus, the loss-of-function and gain-of-function
phenotypes for ids1 seem similar with regard to floret initiation.
This conflicting result can be explained by the function of its redundant
paralog, sid1, which masks the ids1 loss-of-function null
phenotype. Loss of both sid1 and ids1 leads to loss of FM
initiation in the tassel and ear. Therefore, the gain-of-function phenotype of
ids1 (Ts6) shows that it is sufficient for FM initiation,
and the complete loss of function of ids1 and sid1 shows
that it is necessary for FM initiation.
Loss of ids1 and sid1 also results in a reduction in the
number of lateral meristems that initiate from the inflorescence meristem.
This result seems to indicate a role for ids1 and sid1 in
maintaining the stem cell niche, much like AP2 genes in
Arabidopsis (Aida et al.,
2004; Wurschum et al.,
2006). The use of microRNA-resistant forms of AP2
demonstrated that this property acts through the WUSCHEL
(WUS) pathway, which plays a key role in stem cell maintenance
(Zhao et al., 2007). However,
a simple comparison of the inflorescence meristems of the wild type and
ids1;sid1 mutant (Fig.
4A,H) showed that they were approximately the same size. This
indicates that the more likely function of ids1 and sid1 is
to regulate initiation of lateral meristems in the inflorescence, rather than
regulating stem cell maintenance.
The carpelloid bract defects in ids1-Burr;sid1-mum3 ear spikelets
appear to be caused by ectopic expression of AGAMOUS-like MADS-box
genes in the lateral organs of the spikelet. AP2 mutants in
Arabidopsis display carpelloid sepals owing to ectopic expression of
AGAMOUS in those organs (Drews et
al., 1991). The ids1;sid1 floral organ phenotype
demonstrates that this property is conserved in maize. Interestingly, the
ectopic in situ expression of zag1 and zmm2 was not observed
in the tassel (data not shown), which might indicate that these genes have
divergent functions in the male and female inflorescences, as previously
suggested (Mena et al.,
1996).
The ids1;sid1 tassel does not initiate FMs or floral organs. This
function is unique to maize, because ap2 mutants in
Arabidopsis continue to make flowers. A role for ap2 in FM
fate is seen in double mutants with ap1. Arabidopsis ap2;ap1 mutant
flowers are less determinate, and initiate axillary structures in a helical
pattern that develop as pistils with occasional stamens
(Irish and Sussex, 1990;
Shannon and Meeks-Wagner,
1993). The lfy mutant of Arabidopsis displays
striking similarities to maize ids1;sid1. Both lfy and
ids1;sid1 mutants are indeterminate, initiate several bracts before
terminating in carpel-like structures
(Huala and Sussex, 1992), and
lack expression of B-function genes such as APETALA3/silky1
(Weigel and Meyerowitz, 1993).
The lfy phenotype is most obvious on early-formed flowers and, like
ap2, is enhanced in double mutants with ap1
(Huala and Sussex, 1992;
Weigel et al., 1992;
Shannon and Meeks-Wagner,
1993). Thus, LFY, AP1 and AP2 are all thought to
play a role in the transition from IM to FM in Arabidopsis.
|
). Unlike
ids1;sid1, however, zfl1;zfl2 mutants display indeterminacy
in the carpel and FM, and not in the SM. Moreover, the ids1;sid1
phenotype is distinct in that both FMs and sex organs fail to form. The
uniqueness of the ids1;sid1 phenotype might be due to its effects on
the fate of the SM, which normally initiates sterile bracts before florets are
made. If ids1 and sid1 are required for the SM to transition
to FM initiation, then a block at this step could lead to the formation of
multiple sterile organs. Since floral bracts are present in both
Arabidopsis and maize, these pathways are likely to be parallel in
both monocots and dicots. One intriguing possibility is that the divergence of
monocots and dicots has led the AP2 genes to substitute for
LFY function in the grasses. Analysis of sid1 and
ids1 in other genera closer to the monocot/dicot divide will
elucidate the evolution of AP2 versus LFY genes in FM
fate. ACKNOWLEDGMENTS
We thank D. Hantz for greenhouse maintenance; B. Thompson, N. Bolduc, C. Lunde and H. Candela for helpful comments on the manuscript; and Devin O'Conner for phylogenetic analysis. This work was supported by National Science Foundation (NSF) grant DBI-0604923 and by USDA-ARS Current Research Information System (CRIS) grant 5335-21000-018-00D to S.H., and by Cooperative State Research, Education and Extension Service (CSREES) grant 2004-35301-14507 to G.C.
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