Sex Plant Reprod (1997) 10:6773

Springer-Verlag 1997

R EV I E W

&roles:Hargurdeep S. Saini

Effects of water stress on male gametophyte development in plants

&misc:Received: 31 October 1996 / Revision accepted: 18 February 1997

&p.1:Abstract Male reproductive development in plants is highly sensitive to water deficit during meiosis in the microspore mother cells. Water deficit during this stage inhibits further development of microspores or pollen grains, causing male sterility. Female fertility, in contrast, is quite immune to stress. The injury is apparently not caused by desiccation of the reproductive tissue, but is an indirect consequence of water deficit in the vegetative organs, such as leaves. The mechanism underlying this stress response probably involves a long-distance signaling molecule, originating in the organs that undergo water loss, and affecting fertility in the reproductive tissue, which conserves its water status. Much research has been focused on the involvement of abscisic acid in this regard, but the most recent evidence tends to reject a role for this hormone in the induction of male sterility. Stress-induced arrest of male gametophyte development is preceded by disturbances in carbohydrate metabolism and distribution within anthers, and an inhibition of the key sugar-cleaving enzyme, acid invertase. Since invertase gene expression can be modulated by sugar concentration, it is possible that decreased sugar delivery to reproductive tissue upon inhibition of photosynthesis by stress is the signal that triggers metabolic lesions leading to failure of male gametophyte development. &kwd:Key words Pollen Anther Male fertility Male sterility Water stress Male gametophyte&bdy:

Introduction
Productivity in agricultural ecosystems is severely reduced by various biotic and abiotic stresses (Boyer 1982). The extent to which crop productivity is affected depends largely on the stage of development at which the
H.S. Saini Institut de recherche en biologie vgtale, Universit de Montral, 4101 rue Sherbrooke est, Montral, Qubec, H1X 2B2 Canada Tel. +15148720272; Fax +15148729406; e-mail Sainih@ere.umontreal.ca&/fn-block:

plants encounter stress (e.g. Salter and Goode 1967). Among these stages, reproductive development from meiosis in the spore mother cells to fertilization and early seed establishment is extremely sensitive to various stresses, such as drought (Salter and Goode 1967; OToole and Moya 1981; Saini and Aspinall 1981; Westgate and Boyer 1986), heat (Satake and Yoshida 1978; Saini and Aspinall 1982a; Schoper et al. 1987; Morrison 1993), cold (Hayase et al. 1969; Brooking 1976; Lardon and Triboi-Blondel 1994), flooding (Matsushima 1962; Reddy and Mittra 1985) and nutrient deficiencies (Zavadskaya and Skazkin 1960; Graham 1975; Campbell and Leyshon 1980; Sharma et al. 1987; Azouaou and Souvr 1993). These stresses cause various structural and functional abnormalities in reproductive organs, leading to failure of fertilization or premature abortion of seed or fruit. Thus, the damage to productivity from stress at this stage is particularly severe for crops in which the economic yield is the product of sexual reproduction, as in cereals. Water deficit probably ranks as the most important environmental factor limiting global crop productivity (Fischer and Turner 1978; Boyer 1982). In many crops, particularly cereals, reproductive development is the most water-stress-sensitive period after seed germination and seedling establishment has been accomplished (Salter and Goode 1967). The risk of damage is often quite serious because high sensitivity of reproductive development often coincides with high probability of drought at this late stage, when transpiration rates are high and the soil moisture level is low, especially under rain-fed conditions. Water stress interferes with reproductive success of plants by arresting the development of the male gametophyte and, sometimes, the female gametophyte, preventing fertilization and/or inducing premature abortion of the fertilized ovule (e.g. Moss and Downey 1971; OToole and Moya 1981; Saini and Aspinall 1981; OToole and Namuco 1983; Westgate and Boyer 1986; Sheoran and Saini 1996). Among these effects, the arrest of male gametophyte development leading to pollen sterility is

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common to all the cereals examined, and is the primary focus of this review. Although vulnerability to water stress at this stage has been known since the turn of the century, serious inquiries into the mechanisms underlying the failure of male gametophyte development began only in the early 1980s. The work prior to 1967 was comprehensively reviewed by Salter and Goode (1967) and, therefore, is mentioned here only briefly.

Stages of sensitivity to water stress

Drought during the period from stamen initiation to anthesis causes serious yield reduction in many cereal and dicot crops (Sato 1954; Wells and Dubetz 1966; Salter and Goode 1967; Dubetz and Bole 1973; Fischer 1973; Lewis et al. 1974; OToole and Moya 1981; Mahalakshmi et al. 1987; Craufurd et al. 1993; Turner 1993; Westgate and Peterson 1993; and the references cited therein). Two peaks of sensitivity are encountered within this period. The first, which appears to be common to all the cereals examined, is centered around the period from meiosis to tetrad break-up in anthers. This window of sensitivity has been determined quite precisely in wheat and rice (Bingham 1966; Saini and Aspinall 1981; Namuco and OToole 1986; Dembinska et al. 1992; Sheoran and Saini 1996), and is probably identical in barley, oats and maize (Kisselbach 1950; Salter and Goode 1967; Downey 1969; Moss and Downey 1971). In the female tissue, this period corresponds to meiosis in the megaspore mother cell and the subsequent degeneration of three redundant megaspores in the tetrad (Bennett et al. 1973). The second peak of sensitivity occurs during anthesis and initial stages of grain development, and is conspicuous in rice, maize and some dicots (Claassen and Shaw 1970; Hsiao 1982; OToole and Namuco 1983; Schoper et al. 1986; Westgate and Boyer 1986; Ekanayake et al. 1989; Ekanayake et al. 1990; Turner 1993; Westgate and Peterson 1993; and the references cited therein). Some sensitivity at this stage, particularly when the stress is severe, has also been observed in wheat, barley and oats (Aspinall et al. 1964; Wardlaw 1971; Fischer 1973; Sandhu and Horton 1977; Brocklehurst et al. 1978). In several other grasses, such as rye, millet and sorghum, which are damaged by water deficit during the broad period from flower development to just after fertilization, the precise stage of sensitivity is not known (Salter and Goode 1967; Lewis et al. 1974; Mahalakshmi and Bidinger 1985; Mahalakshmi et al. 1987; Craufurd et al. 1993).

The nature of injury to male reproductive organs

The nature of injury to male reproductive organs depends on the stage at which the plant experiences water stress. Meiotic-stage stress affects the subsequent development of the male gametophyte, as will be discussed later. Stress during anthesis and early grain development caus-

es a variety of abnormalities in floral organs which interfere with pollination or fertilization, and induces abscission of flowers or abortion of newly formed grains (Herrero and Johnson 1981; OToole and Namuco 1983; Westgate and Boyer 1986; Ekanayake et al. 1989; Ekanayake et al. 1990; Turner 1993; Westgate and Peterson 1993; and references cited therein). These effects of stress are not within the scope of this review, because the male gametophyte has already developed to maturity by this stage. Water stress at the meiotic stage induces pollen sterility in wheat (Skazkin 1961; Saini and Aspinall 1981), barley (Skazkin and Zavadskaya 1957; Zavadskaya and Skazkin 1960), oats (Novikov 1952), rice (Sheoran and Saini 1996) and maize (Downey 1969). Wheat and rice plants stressed at this stage produce small and shriveled anthers that do not dehisce (Saini and Aspinall 1981; Sheoran and Saini 1996). All pollen in such anthers, and a variable proportion of pollen in the apparently normal anthers, is sterile. Developmental abnormalities in anthers upon exposure to water deficit during meiosis have been studied in wheat (Saini et al. 1984; Lalonde et al. 1997). Microspore mother cells apparently complete meiosis, but further microspore development is arrested at various stages. The most common and conspicuous sign of developmental failure is the dislocation of microspores from their normal peripheral position. This can happen at any time between the young microspore stage and the first pollen grain mitosis; the timing apparently depends on the cultivar. In some anthers, abnormal vacuolization of the tapetum can be seen soon after meiosis. Thus, it is possible that tapetal dysfunction leads to the loss of microspore orientation (Lalonde et al. 1997). The disoriented pollen grains have dilute cytoplasm, little or no intine but normal exine, and they fail to accumulate starch, which is a major constituent of fertile grass pollen (Saini and Aspinall 1981; Saini et al. 1984; Dorion et al. 1996; Franchi et al. 1996; Sheoran and Saini 1996; Lalonde et al. 1997). The female gametophyte is often not affected at all by stress levels that seriously reduce pollen fertility (Bingham 1966; Saini and Aspinall 1981). Injury to the female gametophyte has been observed only in a few instances where the stress was severe and prolonged (Skazkin and Lukomskaya 1962; Moss and Downey 1971). Female fertility may indeed be generally tolerant to stress, because heat and low temperature also induce extensive male sterility but have no or only minor effect on female fertility (Hayase et al. 1969; Brooking 1976; Satake and Yoshida 1978; Saini and Aspinall 1982a; Saini et al. 1983). The greater stress-tolerance of the female gametophyte is of adaptive significance. In the field, the potential reduction in grain set due to pollen sterility could be offset by cross-pollination, owing to an excess of pollen produced and the varying degrees to which male fertility is affected in different florets (e.g. Saini and Aspinall 1981). However, a reduction in female fertility could not be overcome.

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Relationship between tissue water deficit and sterility

In wheat plants subjected to water stress for 34 days during the period that includes meiosis, grain set (an indirect measure of male fertility) was not affected until xylem water potential (w) fell to 1.2 MPa (Fischer 1973). Grain set declined linearly with further decline in w to reach zero at xylem w of 2.4 MPa. In other experiments, decline in w to 2.3 MPa over 9 days, compared to 0.8 MPa in controls, was associated with a 35% reduction in grain set (Saini and Aspinall 1981). A more rapid water stress of similar magnitude caused slightly greater damage to grain set (Dorion et al. 1996). These stress levels lie between moderate and severe for wheat. Decline in grain set of rice by a stress of similar severity ranged from approximately 40%78%, with a wide genotypic variation (Namuco and OToole 1986; Garrity and OToole 1994; Sheoran and Saini 1996). When wheat or rice plants are water-stressed during meiosis, w in the inflorescence or floral organs either does not change (Saini and Aspinall 1981) or declines much less than in the leaf (Morgan and King 1984; Tsuda and Takami 1993; Dorion et al. 1996; Westgate et al. 1996). This relative immunity of the meiotic-stage inflorescence to water loss could be due to the fact that it is enveloped within two or more leaf sheaths (Saini and Aspinall 1981; Sheoran and Saini 1996). Thus, transpiration from the inflorescence would be minimal at this time. This, combined with a break in xylem in the basal part of the floret, which probably causes a hydraulic discontinuity (Zee and OBrien 1970; OBrien et al. 1985), could be the reason for the lag between the drop in w of vegetative (e.g. leaf) and floral parts of stressed plants. Bradford (1994) suggested that apparent constancy of w in developing seeds despite large changes in w of the maternal tissue a situation analogous to that of preanthesis spikelets could be attributed to the ability of excised seeds to regulate solute compartmentation during the long incubation periods in psychrometric measurements. Although this calls for caution in interpreting the w data obtained with a psychrometer, rapid measurements with a pressure chamber also show that spike w remains constant and much higher than leaf w during stress (Saini and Aspinall 1981). Even when the w of spikelets, anthers or ovaries of water-stressed plants does decline, the decline is fully matched by a reduction in osmotic potential (s), preventing any change in spikelet turgor while leaf turgor drops to zero (Morgan 1980; Morgan and King 1984; Westgate et al. 1996). Thus, water-stress-induced reduction in grain set does not correlate with the water status of the reproductive structures. Further, fertility declines only after leaf turgor falls to zero (Morgan 1980; Morgan and King 1984).

How does the reproductive tissue sense water stress? Role of a transportable sporocide
The foregoing observations indicate that water-stress-induced male sterility is unlikely to be a result of desiccation of reproductive structures (Morgan 1980; Saini and Aspinall 1981). Instead, it is probably caused by indirect consequences of a drop in w or turgor elsewhere in the plant, which is somehow communicated to the reproductive tissue. How? The fact that grain set does not decline until leaf turgor falls to zero (Morgan 1980) suggests the involvement of a turgor-responsive phenomenon, such as the accumulation of abscisic acid (Aspinall 1980; Pierce and Raschke 1980; Walton 1980). Hence, the idea that abscisic acid (ABA) produced upon turgor loss in vegetative tissues (e.g. leaf) is translocated to the inflorescence, where it triggers events leading to male sterility, has been the subject of much research. Several pieces of evidence favor this hypothesis: (1) Meiotic-stage spikelets and anthers accumulate ABA during water stress despite no change in their turgor (Morgan 1980; Saini and Aspinall 1982b; Westgate et al. 1996), indicating that the hormone is transported from leaves or other vegetative tissues. Long-distance transport of ABA to spikes in wheat, and in other species, has been demonstrated (Goldbach and Goldbach 1977; Wolf et al. 1990). (2) Application of exogenous ABA to the spike or leaf causes pollen sterility and loss of grain set in wheat (Morgan 1980; Saini and Aspinall 1982b; Waters et al. 1984; Zeng et al. 1985). (3) Spikelet ABA-content upon ABA application is within the same order of magnitude as that in water-stressed plants, when the two treatments produce similar levels of sterility (Saini and Aspinall 1982b). Grain set correlates negatively and tightly with ABA levels in anthers, ovaries and glumes of water-stressed wheat plants (Westgate et al. 1996). (4) Applied ABA and water stress both have maximal effects during meiosis (Morgan 1980; Saini and Aspinall 1981; Saini and Aspinall 1982b; Morgan and King 1984; Zeng et al. 1985). (5) Both treatments reduce grain set by inducing male sterility without affecting female fertility (Saini and Aspinall 1982b). (6) Anthers and pollen grains affected by stress or ABA look morphologically similar at maturity (Morgan 1980; Saini and Aspinall 1981; Saini and Aspinall 1982b). (7) Consistent with these observations, differences in seed set between well-watered plants of two cultivars of wheat relate inversely to the ABA content of the spike (Morgan and King 1984), a nuclear-male-sterile mutant of wheat has a greater ABA level and a lower rate of ABA metabolism in spike and leaves than the corresponding fertile plants (Zeng and King 1986), and distal florets within a wheat spikelet set fewer grains and contain higher ABA levels than the more fertile basal florets (Lee et al. 1988).

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The above correlations do not provide any evidence of a causal role of increased ABA level in the induction of male sterility in stressed plants. A major difficulty in addressing this issue is the lack of a specific inhibitor of ABA biosynthesis or action. Taking an alternative approach, Dembinska et al. (1992) used wheat plants with root systems split into two equal halves to subject half the roots to water stress while keeping the other half wet. Water uptake by the wet half maintained normal leaf w, while ABA content of the spike increased, presumably via transport from dry roots, to the level measured in plants with the entire root system stressed. However, sterility was induced only with the entire root system stressed, which also caused leaf w to decline. Thus, increased ABA level in the spike could not be the sole regulator of fertility, a view also supported by an earlier observation of developmental differences between ABAand water-stress-affected anthers (Saini et al. 1984). Among the questions not answered by the work of Dembinska et al. (1992) is whether it is possible that ABA arriving in the reproductive tissue from the roots and leaves could be differentially compartmentalized. It is also possible that an interaction between ABA and some other consequence(s) of reduced w is required to cause sterility, as indeed seems to happen in the regulation of stomatal aperture (Tardieu and Davies 1992). On the other hand, and on a cautionary note, the focus on the role of ABA in this stress response is rooted largely in the initial observation that ABA application induces male sterility (Morgan 1980). Yet, the sporocidic effect of ABA is not unique, since a variety of synthetic and natural substances induce sterility in plants (McRae 1985; Cross and Ladyman 1991; Sawhney and Shukla 1994). Moreover, stresses that do not affect tissue ABA levels can also cause nearly complete sterility (Saini and Aspinall 1982b). Hence, apparent similarities among the effects of chemicals and stress on pollen fertility may simply be a reflection of the limited range of vulnerable events during reproductive development rather than a similarity in the underlying mechanisms. Could other hormones be involved in the stress response? Cytokinins influence a variety of developmental processes, and water stress can affect cytokinin levels in plants (Aspinall 1980; Davies et al. 1986; Davies and Zhang 1991). Application of cytokinins can prevent heatinduced kernel abortion in maize and improve flower production and fruit set in other species (Carlson et al. 1987; Atkins and Pigeaire 1993; Mosjidis et al. 1993; Cheikh and Jones 1994). Pressurizing the roots of waterstressed wheat plants prevents browning of apical spikelets, a potential symptom of increased cytokinin level, and improves fertility (Westgate et al. 1996). Thus, the possible involvement of cytokinins in the control of fertility in water-stressed plants merits further investigation. Ethylene was also hypothesized as a stress-induced sporocide (Morgan 1980), but appears unlikely to fit this role because unphysiologically high ethylene concentrations are required to cause male sterility (Bennett and Hughes 1972; Fairey and Stoskopf 1975; Saini 1982)

and water stress does not promote ethylene evolution from intact wheat and other plants (Morgan et al. 1990; Narayana et al. 1991). Signals originating in roots can influence physiological responses of the aerial parts of a plant (Davies and Zhang 1991). The experiments with split-root systems indicate that it is unlikely that the hypothetical male sporocide originates in roots (Dembinska et al. 1992). Pressurization of roots of water-stressed plants to maintain leaf w at the level of well-watered plants improved grain set compared to un-pressurized stressed plants, indicating that shoot w is a more important determinant of grain set than the root w (Westgate et al. 1996).

Cellular and metabolic bases for the failure of male gametophyte development
Initial attempts to understand the reasons for the male sterilant effect of water stress found abnormalities in chromosomal pairing and separation during meiosis in pollen mother cells of rather severely stressed barley (Skazkin and Zavadskaya 1957). Namuco and OToole (1986) also reported that a number of meiotic abnormalities in water-stressed rice started to increase at relatively moderate stress (leaf w 1.1 to 1.9 MPa) and peaked when the w was around 2.2 MPa. Whether any of these abnormalities contributed to sterility is not known, although the cessation of meiosis observed under severe stress (leaf w 3.5 MPa) would do so, unless it were reversed after stress (Namuco and OToole 1986). In contrast, no such abnormalities were noticed in wheat (Saini 1982), where meiotic division in stressed plants is nearly always completed (Saini et al. 1984; Lalonde et al. 1997). This also appears to be the case in moderately stressed rice, where microspores are produced but their development fails at later stages (Sheoran and Saini 1996). In wheat, the products of meiotic division, with a few exceptions (Lalonde et al. 1997), continue to develop normally for several days before aborting (Saini et al. 1984; Lalonde et al. 1997). This points to a more subtle lesion than abnormal or failed meiosis as the cause of male sterility. Late in their development, normal grass pollen grains accumulate starch, which is subsequently utilized to support pollen germination and pollen tube growth (MikiHirosige and Nakamura 1983; Pacini and Franchi 1988; Clment et al. 1994; Franchi et al. 1996). Cereal pollen grains sterilized by drought or other stresses lack starch (Ito 1978; Saini and Aspinall 1981; Saini and Aspinall 1982a; Sheoran and Saini 1996). Water stress also changes the pattern of distribution of starch in anthers, and inhibits intine development in pollen grains (Saini et al. 1984; Lalonde et al. 1997). The timing of these events, discussed earlier in this article, suggests that disturbance in carbohydrate availability and/or metabolism may be involved in the failure of pollen development in stressed plants. Several other observations also support this idea. Increased sucrose uptake increases the grain set

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in detached wheat spikes cultured in nutrient solution (Waters et al. 1984). Addition of ABA to the nutrient solution decreases sucrose uptake and grain set, and both effects are reversed by supplementing the medium with additional sucrose. Water stress inhibits the rate of photosynthesis and export of assimilate from the leaves (Boyer and McPherson 1975; Hanson and Hitz 1982), and could thus deprive anthers of sucrose. Paradoxically, wheat and rice anthers accumulate sucrose and other sugars during stress, which would suggest that they are not starved of sucrose (Dorion et al. 1996; Sheoran and Saini 1996). However, this accumulation could be the result of an inhibition of sugar utilization, regardless of the effect of stress on sugar supply to anthers. In wheat anthers, soluble acid invertase activity declines dramatically during meiotic-stage water stress, and never recovers even after the stress is relieved (Dorion et al. 1996; Sheoran and Saini 1996). The effect is quite specific in wheat, where the activities of starch synthase and ADPglucose pyrophosphorylase, and the expression of ADPglucose pyrophosphorylase gene are not appreciably affected by stress (Dorion et al. 1996; Lalonde 1996). In rice, activities of these enzymes decline somewhat during meiotic-stage stress or soon thereafter (Sheoran and Saini 1996). Perhaps the most significant element in these observations is the inhibition of invertase, which is the dominant enzyme of sucrose cleavage in the anthers of many species (Bryce and Nelsen 1979; Nakamura et al. 1980; Nakamura et al. 1992; Dorion et al. 1996; Sheoran and Saini 1996). Reduced invertase activity in anthers would curtail proper processing of incoming sucrose, and the resulting decline in carbon and energy supply could jeopardize crucial metabolic and developmental processes. In wheat, the decline in invertase activity precedes or coincides with the first anatomical signs of pollen abortion (Saini et al. 1984; Dorion et al. 1996; Lalonde et al. 1997). Inhibition of this activity could be the cause of sucrose accumulation in anthers (Dorion et al. 1996), despite the expected sucrose shortage caused by the reduction in photosynthesis (Boyer and McPherson 1975; Hanson and Hitz 1982). Moreover, the redistribution of starch, particularly its accumulation in the connective tissue (Lalonde et al. 1997), is consistent with the inhibition of sucrose utilization by stressed anthers. Diversion of excess sucrose to starch has been demonstrated in Lilium anthers (Clment and Audran 1995). This finding identifies a metabolic lesion that occurs early enough to merit consideration among potential causal events, or, at least, as a point from where to proceed in search of a primary sterility-triggering event.

sucrose synthase, the enzymes that catalyze the critical first step in sucrose metabolism in different tissues, are regulated in this fashion; the expression of different members of these gene families can either be enhanced or repressed by sucrose (Koch et al. 1992; Xu et al. 1996). It appears that differential sucrose-modulation of the expression of these genes in vegetative and reproductive tissues could adjust carbon allocation during development and under stressful conditions (Xu et al. 1996). In this context, the effects of water stress on acid invertase activity in anthers present exciting possibilities for inquiry into the mechanisms of failure of pollen development (Dorion et al. 1996; Sheoran and Saini 1996). Sugar could fit the description of the stress-signaling molecule hypothesized earlier in this article; a decline in photosynthesis at low leaf w could restrict sucrose delivery to the inflorescence, inhibiting the expression of certain invertase genes in anthers. The attendant impact on sugar processing could jeopardize sugar-dependent events in pollen development. The observed sugar accumulation and its re-routing to starch in the cells outside the anther locule is consistent with such a mechanism (Dorion et al. 1996; Lalonde et al. 1997). A similar situation may also exist with regard to water-stress-induced kernel abortion in maize (Zinselmeier et al. 1995), raising the possibility that the mechanisms underlying pollen and kernel abortion could be very similar. The parallels between these two responses to stress have been discussed elsewhere (Saini and Lalonde 1997).
&p.2:Acknowledgements The research in my laboratory cited herein was supported by grants from the Natural Sciences and Engineering Research Council of Canada and the Rockefeller Foundation.

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