Nuclear Genes Controlling Male Fertility - The Plant Cell · The Plant Cell, Vol. 5, 1277-1283, October 1993 O 1993 American Society of Plant Physiologists Nuclear Genes Controlling

The Plant Cell, Vol. 5, 1277-1283, October 1993 O 1993 American Society of Plant Physiologists

Nuclear Genes Controlling Male Fertility Abdul M. Chaudhury CSlRO Division of Plant Industry, GPO Box 1600, Canberra ACT 2601. Australia

INTRODUCTION

In higher plants, the developmental programs of the male and female organs are substantially independent of each other and of the vegetative plant. This developmental independence per- mits the genetic dissection of fertility processes without impairing vegetative growth.

Male fertility requires a number of coordinated developmen- tal events. These include the formation, as part of the flower, of stamens and anthers from the vegetative meristem; the de- velopment of pollen grains inside the anther locules; the timely release and deposition of pollen on the stigma; and finally, in self-compatible plants, the interaction of the male and fe- male gametes to attain self-fertilization. Mutations can be obtained that perturb any of the above processes, giving rise to a plant with impaired pollen function but normal female fer- tility. Such mutations in self-compatible plants have been described as male steriles (ms).

Genetic studies in a wide variety of plants indicate that most of the developmental steps leading to male fertility are con- trolled by nuclear genes. ms mutants are self-sterile but female fertile and, hence, retain their ability to respond to outcross- ing. Whereas some of the male-sterile mutants lack male organs altogether (Hill and Lord, 1989; Coen and Meyerowitz, 1991), others have normal male organs but lack pollen (Kaul, 1988); in a third category, visible pollen is formed that is non- functional. There is also a category of mutants with defective anthers (Hafen and Stevenson 1958; Chaudhury et al., 1992). Other ms mutants are defective in the temporal control of pol- len formation (Kaul, 1988). In this last type of mutant, pollen is formed either to0 early or to0 late for efficient self-fertilization. However, when pollinated by functional pollen from a male- fertile plant, each of these mutants produces as many seeds as normal self-pollinating plants. Pollen from this type of mu- tant is also able to fertilize other plants.

The goal of this review is to describe male-sterile mutants that define nuclear genes controlling male fertility. I shall re- view work done in severa1 plants so as to cover adequately various landmark developmental events. For a more compre- hensive review of male sterility, the reader is referred to Kaul (1 988).

DEVELOPMENTAL STEPS LEADING TO MALE FERTlLlTY

To interpret correctly the phenotypes of male-sterile mutants, it is important to understand the normal developmental events

that lead to male fertility. I shall describe these events for Arabidopsis, for which detailed descriptions of normal flower development are available (Hill and Lord, 1989; Smyth et al., 1990; see Goldberg et al., 1993, this issue, for description of stamen development in tobacco).

Development of Male Sexual Organs

The male sexual organs, the stamens, originate from the flo- ral meristem of the plant. The development of stamens thus occurs after vegetative meristems are converted to floral meristems.

The wild-type Arabidopsis flower consists of four whorls of floral organs, each occupied by a different type of organ (see Coen and Carpenter, 1993, this issue). Whorl 1 contains four sepals; whorl 2, four petals; whorl 3, six stamens; and whorl 4, two fused carpels forming an ovary. The male sexual part of the flower consists of the six third whorl stamens, four long and two short, each comprising an anther and a filament (Smyth et al., 1990).

The stamen primordia first become visible, together with the peta1 primordia, after the formation of the floral buttress and the sepal primordia (Smyth et al., 1990). The primordia of the four long stamens are seen as wide outgrowths of the central dome of cells. lnitiation of the two short stamens occurs op- posite each lateral sepal slightly after the initiation of the long stamens. Later, the stamen primordia become stalked toward their bases, thus separating the lower part of each stamen, which becomes the filament, from the upper part, which differentiates into the concave protrusions of the anthers. The filaments then elongate in concert with the gynoecium such that during anthesis, a copious amount of pollen is deposited on the stigma.

Development of Pollen Grains

Successful pollen development comprises three major de- velopmental stages: sporogenesis, or the differentiation of the sporogenous cells and meiosis; the postmeiotic development of free microspores; and microspore mitosis, including the di- vision of the generative nucleus to form the two sperm of mature pollen (see McCormick, 1993, this issue).

Sporogenesis takes place inside anther locules, whose de- velopment is discussed by Goldberg et al. (1993, this issue). The tapetum is the innermost layer of the anther wall. It

1278 The Plant Cell

completely surrounds the sporogenous tissue and plays animportant role in microspore development (for review, seeBhandari, 1984; Pacini et al., 1985). Tapetal expression of aribonuclease gene in transgenic plants leads to a block in pol-len development and to male sterility, underscoring theimportance of the tapetal cells (Mariani et al., 1990; Goldberget al., 1993, this issue). During prophase of the meiotic divi-sion of the sporogenous cells, the tapetal cells undergo nucleardivision without cytokinesis and or endomitosis, leading to highDMA content. The tapetum also produces the enzyme callase,which degrades the walls of the microspore tetrads that arethe products of meiosis, releasing free microspores.

After microspores are released from the tetrads, sporopolle-nins produced by the disintegrated tapetum are deposited onthe outer walls of the released microspores. Tapetally derivedmaterial, such as flavonols deposited on the outer walls of thepollen grains, are thought to be important for pollen germina-tion and pollen-stigma interactions (Mo et al., 1992; also seebelow). Thus, any alterations in the constituents of the tape-tum might interfere with pollen-stigma interactions and leadto male sterility. Many of the meiotic processes that occur dur-ing microsporogenesis and megasporogenesis are similar andare therefore under joint genetic control. This is shown by thefact that many meiotic mutants show both male and femalesterility. However, there are a number of male-sterile, female-fertile mutants in which the defect is meiotic, indicating thatportions of male meiosis are under separate genetic control.Alternatively, male meiosis could be more sensitive than fe-male meiosis to reduction in the products of certain genes.

MALE-STERILE MUTANTS OF HIGHER PLANTS

mutant antherless (at) has normal filaments but lacks anthers(Weijer, 1952; Kaul, 1988). In the gibberellin (GA)-deficient dwarfmutants d2, d3, and d5 and in the anther-ear mutants anl andan2, smaller-than-normal anthers develop that are devoid ofpollen (Duvick, 1965; Kaul, 1988). In a dominant mutant of cot-ton, ms4, stamens are differentiated but anthers are malformed(Allison and Fisher, 1964). In the Arabidopsis at mutant, shownin Figure 1, filaments are present but anther lobes are eithernot fully differentiated or are converted to sepals (Chaudhuryetal., 1992). This mutant, apart from having abnormal stamens,also lacks petals and has an altered inflorescence (A.Chaudhury and S. Craig, unpublished observations), indicat-ing that this gene is required not only for anther formation butalso for other floral processes.

Mutants have also been described in which filaments failto elongate, thus giving rise to male sterility. For example, anauxin-resistant Arabidopsis mutant has been reported thatfails to self-pollinate because the anther filaments are substan-tially shorter than the silique at anthesis. This mutant impli-cates auxins in controlling filament elongation (Estelle andSomerville, 1987). A tomato mutant, stamenless-2, has beendescribed in which stamens are shorter and paler in color thanwild-type stamens (Sawhney and Bhadula, 1988). Undernormal growth conditions, the mutant anthers produce non-functional microspores. However, the addition of the plantgrowth regulator GAs can restore pollen function. This resultindicates that GAs may play a role in stamen development(Sawhney and Greyson, 1973; Sawhney and Bhadula, 1988).Perhaps a flower-specific production of GA that is absent inthese mutants is required for the expression of critical anther-specific genes.

Mutants That Perturb Male Sexual Organs

Mutations that impair the formation of male sexual organs, butdo not impair the formation of female sexual organs can bedefined as structural male-sterile mutants. In a wide varietyof plants, mutants have been described that alter the ontogenyof male structural organs. In Arabidopsis, the homeotic muta-tions pistillata (pi) and apetala-3 (ap3) affect the identity of petalsand stamens, replacing them with sepals and carpels, respec-tively. As a result, these mutants are male sterile but femalefertile (Bowman etal., 1989; Hill and Lord, 1989). In the pi mu-tant, meristematic cells that would normally produce stamensshow developmental divergence near the time of normal sta-men initiation. The PI and AP3 genes have been cloned andfound to encode members of the MADS family of transcrip-tion factors (Jack et al., 1992; K. Goto and E. M. Meyerowitz,personal communication; see also Coen and Carpenter, 1993,this issue).

Mutants are also known in which stamens develop but nosporogenous tissue is formed. In maize, the recessive nuclear

Figure 1. The antherless Mutant of Arabidopsis.

(A) A wild-type Arabidopsis flower with normal anthers (arrowhead).(B) An anther/ess (at) mutant flower. In the at mutant, anthers are ei-ther absent (not shown) or are converted into sepals (arrowhead), asin the flower pictured here.

Nuclear Genes Controlling Male Fertility 1279

Mutants That Impair Pollen Development

Premeiotic and Me/otic Mutants

Male-sterile mutants that are impaired in microspore develop-ment can be separated into two broad categories, those thathave normal microspore tetrads, and, by implication, normalmeiosis, and those in which microspore tetrads are aberrant,suggesting a premeiotic or meiotic defect. The Arabidopsismutants ms3, ms4, ms5, and ms15 have normal archespor-ial cells but the tetrads are aberrant, as shown in Figure 2(Chaudhury et al., 1992). Thus, the defect in these mutantsis likely to be either premeiotic or meiotic. Table 1 describessignificant male-sterile mutants of Arabidopsis.

Recently, an Arabidopsis mutant, ms2, has been identifiedby tagging with a maize transposable element (Aarts et al.,1993). Anther locules in this mutant are devoid of pollen. Inyoung anthers, the tapetal layer appears to be affected, giv-ing rise to pollen abortion shortly after release from the tetrads.The MS2 gene sequence reveals a short region of homologywith an open reading frame in the wheat mitochondrial ge-nome. Mitochondrial genome rearrangements are oftenassociated with cytoplasmic male sterility (CMS; see Levings,1993, this issue). However, ms2 is a nuclear mutation, and thesignificance of its homology remains unknown.

The Arabidopsis mutants msW and msY are also defectivein meiosis as part of a general disruption of early events inpollen development (Dawson et al., 1993). Detailed cytogeneticanalyses of the Arabidopsis mutants have not been done; thus,it is not known which stage of meiosis is defective. In the tomatomutants ms3, ms15, and ms29, meiosis does not occur, andmostly degenerated pollen mother cells (PMCs) are formed(Rick, 1948), indicating a role for the affected genes inpremeiotic or meiotic sporogenesis. In a cytological study of13 male-sterile mutants of maize, only two, ms8 and ms9, werefound to have abnormal microspore mother cells, indicatingthat premeiotic and meiotic mutants are a minority among male-sterile maize mutants (Albertsen and Phillips, 1981). In ms8mutants, PMC abnormalities occur as early as the leptotenestage of meiosis. PMCs are smaller than normal and often havepoorly delineated margins. Released microspores tend toclump and are small and irregularly shaped. Most of thesemicrospores degenerate quickly without further development.In ms9 mutants, PMCs are also smaller than normal, indicat-ing a premeiotic defect. The first and the second cytokinesisafter meiosis also do not take place.

The maize mutant ms17 has defects including excessmicrotubules, abnormal spindle formation, and improper chro-mosome segregation (Staiger and Cande, 1991). Theseobservations have been interpreted to indicate a positive roleof the normal MS17 product in maintaining microtubule stabil-ity during meiosis.

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Figure 2. Impaired Microsporogenesis in Male-Sterile Mutants ofArabidopsis.

(A) Cross-section of an anther of a male-fertile plant.(B) Cross-section of an ms4 anther. Pollen development is aberrant.(C) Cross-section of an ms3 anther. The locules collapse at the timeof microspore release from the tetrads.

1280 The Plant Cell

Postmeiotlc Mutants

In a number of higher plants, male-sterile mutants have been described in which microspore development is arrested after meiosis, indicating a prominent role of sporophytic genes in controlling postmeiotic microspore development (van der Veen and Wirtz, 1968; Albertsen and Phillips, 1981; Chaudhury et al., 1992). For example, in the Arabidopsis mutant ms7, micro- spores are released from phenotypically normal tetrads, but these subsequently become abnormal.

A number of maize mutants have also been described in which the defect occurs after meiosis (Albertsen and Phillips, 1981). In the mutants ms2 and ms7; microsporogenesis is nor- mal until the tetrad stage, after which chromosomes become condensed precociously. In addition, the microspore walls are thinner than in normal microspores. Meiosis and callose for- mation are normal in these two mutants. Microspores of ms7O and ms73, on the other hand, develop abnormally thickened microspore walls after they are released from tetrads. In the mutant ms72, microspore wall development is normal but nu- clear development is arrested. In this mutant, the nucleus and cytoplasm are degraded but the microspore walls remain well- developed in older anthers, indicating that the gametophyte nucleus is not involved in exine formation. The mutant ms6 is an allele of a previously characterized mutant polymitotic @o). In this mutant, for which three alleles are now available, the postmeiotic mitosis that normally accompanies pollen grain formation begins precociously at the tetrad stage (Kaul, 1988). The latest acting postmeiotic maize mutants are ms5, ms77, and ms74. In these mutants, microspore development is arrested at the microspore mitosis stage (Albertsen and Phillips, 1981).

The purine salvage pathway enzyme adenine phos- phoribosyl transferase, which converts adenine to AMP, has an important function during microspore development in Arabidopsis (Moffatt and Somerville, 1988). A mutant (apt) defi- cient in this enzyme has normal vegetative morphology,

somewhat retarded growth, and is male sterile due to abor- tion of pollen development following the release of microspores from the tetrads (Regan and Moffatt, 1990). It has been pro- posed that the abortion of pollen development in adenine phosphoribosyl transferase-deficient mutants could be due to the toxic accumulation of adenine and its intermediates, or, alternatively, that an aberrant cytokinin metabolism in the apt mutant impairs microspore development through an undefined mechanism (Moffatt et al., 1991).

Pollen Release Mutants

The release of pollen from the mature anther is also under genetic control. In Arabidopsis, a mutant, msH, has been iso- lated in which functional pollen grains inside the anther locules are not released because of a defect in anther dehiscence. The MsH gene may, directly or indirectly, influence aspects of anther wall anatomy required for rupture and opening out of the stomium after pollen maturation (Dawson et al., 1993). In the tomato mutant ps, the anther fails to dehisce (Larsen and Paur, 1948). Mutants have also been reported in barley (Roath and Hockett, 1971) and tomato (Roever, 1948) in which anther dehiscence is inhibited, indicating a role for these genes in anther dehiscence. Some of these mutants might be im- paired in stomium function; stomium rupture is oneof the events that is essential for anther dehiscence (Goldberg et al., 1993, this issue).

Pollen Function Mutants

Severa1 Arabidopsis mutants have been characterized in which genes under sporophytic control alter the interaction of the pollen with the stigma (R. Pruitt, personal communica- tion). Although these mutants produce abundant pollen grains that fail to germinate in vivo, in every case the pollen

Table 1. Male-Sterile Mutants of Arabidopsis

lmpaired Fertility Component Mutation Phenotype Reference

Male sexual organs pistillata aP3 antherless axrl

ms3, ms4, ms5, ms15 Microsporogenesis

ms2

Pollen function POP 1

Dehiscence msH

Stamens absent Stamens absent Anthers absent Short filaments Premeiotic or meiotic arrest of

microspore development Postmeiotic; microspores

become aberrant after being released from tetrads

Pollenless Lack of tryphine Anther fails to dehisce

Bowman et al. (1989) Bowman et al. (1989) Chaudhury et al. (1992) Estelle and Somerville (1987)

A.M. Chaudhury (unpublished observations)

A.M. Chaudhury (unpublished observations)

Aarts et al. (1993)

Preuss et al. (1993)

Dawson et al. (1993)

Nuclear Genes Controlling Male Fertility 1281

could be induced to grow pollen tubes by the addition of wild- type pollen, indicating that diffusible products required for an early step in pollen-stigma recognition are missing in these mutants.

A similar mutant has recently been described that has a re- duced amount of tryphine (Preuss et al., 1993). Pollen grains have an inner cell wall, or intine, that is made of pectin and cellulose, and an externa1 wall made of sporopollenin and cov- ered with a substance called tryphine, an extracellular pollen coat made of lipid and proteins. In the tryphine-deficient mu- tant, in vivo pollen germination is impaired, and callose is apparently formed in stigma cells that contact mutant pollen. The phenotype of this mutant indicates a role of tryphine in pollen-stigma interactions.

Pollen function also appears to require chalcone synthase activity. Maize mutants deficient in chalcone synthase produce nonfunctional pollen (Coe et al., 1981), presumably due to a lack of flavones, which are required for pollen germination. Chalcone synthase, a key enzyme in flavonoid biosynthesis, catalyzes the formation of 2,4,4,6-tetrahydroxychalcone, which is converted, via naringenin, to kaempferol. In petunia, an- tisense suppression of chalcone synthase gene expression led to the formation of nonviable nongerminating pollen (Taylor and Jorgensen, 1992; van der Meer et al., 1992). Microscopic ObSeNatiOn of pollen from chalcone synthase-deficient mu- tants indicates that self-sterility is caused by the failure to produce a functional pollen tube. However, chalcone syn- thase-deficient mutant pollen were found to be partially functional on wild-type stigmas (Mo et al., 1992). The self-sterile phenotype could also be rescued by the addition of micromo- lar quantities of the flavonol kaempferol (Mo et al., 1992). The kaempferol critical for male fertility is of tapetal origin, although it can also be supplied by the stigma, as the results of Mo et al. (1992) show.

Gametophytic Mutants That lmpair Self-Fertility

Most of the nuclear male-sterile mutants that have been de- scribed are sporophytic in their mode of inheritance and action. In this type of sterility, the Mslms heterozygous plant carries only normal pollen; as a result, the ms trait can be passed on to the next generation. By contrast, in gametophytic steril- ity, half of the pollen (the ms pollen) from an Mslms plant is nonviable; thus, the gametophytic sterility trait can be transmitted only through the female. When sporophytic male- sterile mutants are isolated after mutagenesis, mutant plants are screened at the M2 generation. If a mutation conferring gametophytic sterility were to arise, the nonviable pollen would preclude the detection of the mutant in the M2 generation. Thus, to recover mutations that impair gametophytic fertility, pollen from mutagenized M1 plants will have to be screened for 50% nonviability.

In maize, control of gametophytic fertility has been shown for Rf3, a maize fertility restoration factor specific for cms-S cytoplasm (for review of CMS, see Levings, 1993, this issue).

In plants carrying S cytoplasm, rf3 behaves as agametophytic male-sterile mutation. That is, in contrast to the sporophytic Mslms heterozygote, in which all pollen is functional, in Rf3lrf3 plants carrying S cytoplasm, only half of the pollen grains are functional (Laughnan and Gabay, 1973).

Some of the genes that have been isolated based on their gametophytic mode of expression might be important for pollen viability. Promoters from two tomato genes under gametophytic control (LAT52 and LAT59) have been fused to the reporter gene gusA. Studies of these transgenic plants indicated that the GUS activity was under the control of the haploid genome, i.e., in the heterozygous plant, half of the pollen showed GUS activity (Twell et al., 1990; see McCormick, 1993, this issue). lnactivation of these gene(s) by antisense technology should reveal whether their gametophytic expression is required for fertility.

Organismic Phenotypes of the Male-Sterile Mutants

Male sterility causes a number of developmental changes in the plant. Seven Arabidopsis male-sterile mutants were examined for a sporophytic phenotype (A. Chaudhury, unpub- lished observations). All seven mutants had increased numbers of flowers and delayed apical senescence. In addition, in wild- type Arabidopsis, the raceme does not normally produce a terminal flower. By contrast, in each of the male-sterile mutants examined, a terminal flower with developmental abnormali- ties was observed.

The delayed apical senescence, greater number of flowers, and formation of terminal aberrant flowers in the male-sterile mutants are likely to be the result of the lack of fertilization rather than an absence of specific gene functions, because these phenotypes have been observed in a number of male- sterile mutants and can be reversed by outcrossing. Fertiliza- tion is known to cause the release of growth hormones such as GAs and auxins (reviewed in Pharis and King, 1985). These hormones rnight play an important role in fertile plants in con- trolling the number of flowers. It has been reported that male-sterile plants have a higher leve1 of cytokinins than male- fertile plants (Musgrave et al., 1986), presumably due to the lack of fertilization in these mutants.

EVOWTIONARY SlGNlFlCANCE OF THE MS GENES

Nuclear genes controlling self-fertility have played an impor- tant role in the evolution of flowering plants. Herrnaphrodite plants constitute ~ 8 5 % of all angiosperms. Thus, the control of male and female fertility in the same flower must offer a selective advantage over other modes of reproduction. Self- fertilization is very efficient at generating large numbers of seeds without the necessity of a pollen transfer system. On the other hand, an organism that is obligately self-fertilizing would incur inbreeding depression due to the expression of

1282 The Plant Cell

deleterious genes in the homozygous state. Thus, in many plants, genetic or epigenetic inactivation of male fertility en- sures that outcrossing occurs along with self-fertilization. One way this occurs in nature is via mutation of the nuclear genes that control male fertility (see Dellaporta and Calderon-Urrea, 1993, this issue). The resulting population would contain both hermaphrodite and male-sterile members. Dawin detected this phenomenon in a large number of species and termed it gy- nodioecy. That gynodioecy persists in many plant species indicates that the inactivation of nuclear genes is an impor- tant way by which self-fertility is controlled in nature.

SlGNlFlCANCE AND FUTURE DIRECTIONS OF MUTANT ANALYSIS

A large number of male-sterile mutants have been obtained in a number of angiosperms. The many loci identified and their phenotypic diversity indicate that male fertility is a complex developmental process involving many tissue types and coor- dination of a large number of genes. lsolation of these genes will usher in an era of molecular analyses of male fertility.

What are these genes likely to encode? The early acting genes required for the elaboration of male organ identity might encode transcription factors specifically required for the de- termination of the stamen primordia as well as downstream genes that are required for the determination of various an- ther cell types for the elongation of the filament. The identity of these genes remains unknown.

The sporogenous male-sterile mutants are likely to define genes that trigger the archesporial cells to becoms sporogenous; some of these genes are likely to define mem- bers of the transduction chain that initiates sporogenesis. Genes required for the function of the tapetum and male- specific meiosis are likely to constitute the vast majority of the sporogenous male fertility genes. A large number of tapetum- and anther-specific genes have already been isolated based on their tissue-specific expression in tapetum or pollen (Twell et al., 1990; see Goldberg et al., 1993, this issue; McCormick, 1993, this issue). By joining the promoters of these tissue- specific genes with reporter genes such as GUS, in vivo probes for the function of the male-sterile mutants can be constructed. For instance, by creating transgenic plants carrying fusion genes in which GUS expression is controlled by a tapetum- specific promoter, mutants can be screened for that impair the formation of trans-acting factors required for tapetum-specific gene expression.

Although some aspects of the function of the MS gene prod- ucts can be inferred from genetic studies, a molecular understanding of their biochemical function genes must await their molecular cloning. Two different approaches have been taken in Arabidopsis to clone the male-fertility genes: chro- mosome walking and gene tagging. For instance, two groups are attempting to clone the male-sterile msl gene by chromo- some walking.

The second method for the isolation of MS genes in Arabidopsis involves tagging genes with T-DNA (Feldmann and Marks, 1987) or by introducing the maize Ac or other trans- posable element into the Arabidopsis genome (Schmidt and Wilmitzer, 1989; Aarts et al., 1993). In the T-DNA tagging experiment, a large number of reduced fertility mutants have been generated (Feldmann, 1991). Experiments are now un- derway in a number of laboratories to characterize these mutants further to determine whether a T-DNA is linked to the male-sterile phenotype. Once the cosegregation of male sterility and T-DNA is demonstrated, it should be possible to clone the corresponding gene by using the adjacent introduced DNA as a probe. Similarly, transformants of Arabidopsis have been generated in which a modified Ac element is active. Mutations to male sterility that arise in these lines should be tagged and, therefore, clonable.

ACKNOWLEDGMENTS

I thank Liz Dennis for constant encouragement and support, Stuart Craig for the pictures of the ms mutants, and Bob Goldberg and Becky Chasan for their comments on this manuscript.

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DOI 10.1105/tpc.5.10.1277 1993;5;1277-1283Plant Cell

A. M. ChaudhuryNuclear Genes Controlling Male Fertility.

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