Drought is a multidimensional stress affecting plants at various levels of their organization. The effect of and plant response to drought at the whole plant and crop level is most complex because it reflects the integration of stress effects and responses at all underlying levels of organization over space and time. This review discusses some of the major aspects of crop response to drought stress which are relevant for plant breeding. Emphasis is given to whole plant aspects which are too often disregarded when conclusions are drawn from molecular studies towards the genetic improvement of crop drought resistance. Topics discussed are seedling emergence and establishment, plant phenology, leaf area, water deficit and assimilation, osmotic adjustment, the root and the formation of yield. The discussion is concluded with the interpretation of crop adaptation to drought conditions in its agronomic sense. Conclusions are drawn regarding plant breeding for drought-prone conditions.

Crop responses to drought and the interpretation of adaptation

Reproductive development of plants is highly vulnerable to water deficit. Stress early during this phase can delay or completely inhibit flowering, both through an inhibition of floral induction and development. The stage of meiosis is perhaps the most stress-sensitive period of reproduction in all species studied. A meiotic-stage water deficit causes pollen sterility, but usually affects female fertility only under extreme stress. Sterility occurs even though the reproductive structures of stressed plants maintain a high water status, indicating that the response is probably mediated by a sporocidal signal from elsewhere in the plant. Rice and maize plants are also highly vulnerable during flowering (anthesis) and early grain initiation. Stress during this period can cause loss of pollen fertility, failure of pollination, spikelet death, or zygotic abortion. Changes in carbohydrate availability and metabolism appear to be involved in the effects of stress during meiosis and anthesis. Stress during early grain development curtails the kernel sink potential by reducing the number of endosperm cells and amyloplasts formed. Controls underlying these effects are poorly understood, although hormones may be involved. A water deficit during any stage of grain development causes the premature cessation of grain filling. Kernel moisture content and its direct impact on metabolism appear to be key regulatory factors in shortening the duration of grain filling.

Reproductive Development in Grain Crops during Drought

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.

Effects of water stress on male gametophyte development in plants

Water deficit during meiosis in pollen mother cells of wheat (Triticum aestivum L.) induces male sterility, which can reduce grain set by 40 to 50%. In plants stressed during meiosis and then rewatered, division of pollen mother cells proceeds normally but subsequent pollen development is arrested 3 or 4 d later. An inhibition of starch accumulation within the pollen grain suggested that an alteration in carbohydrate metabolism or assimilate supply may be involved in pollen abortion. We measured levels of various carbohydrates and activities of key enzymes of Suc metabolism and starch synthesis at different stages of pollen development in anthers collected from well-watered and water-stressed plants. Compared to controls, soluble sugars increased in anthers stressed during meiosis, then decreased at later poststress stages. Sucrose and myoinositol accounted for part of the sugar accumulation. The activity of soluble acid invertase declined 4-fold during the stress period and never recovered thereafter. Sucrose synthase activity during starch accumulation in pollen was also lower in the anthers of plants stressed at meiosis. Stress had little negative effect on the activities of ADP-glucose pyrophosphorylase or soluble and granule-bound starch synthase during starch accumulation in pollen, although at the earlier stages, ADP-glucose pyrophosphorylase activity in stressed anthers was slightly lower compared to controls. The results suggest that carbohydrate starvation per se and inhibition of the enzymes of starch synthesis probably were not responsible for the stress-induced pollen abortion. Instead, an inability to metabolize incoming sucrose to hexoses may be involved in this developmental lesion.

Induction of Male Sterility in Wheat by Meiotic-Stage Water Deficit Is Preceded by a Decline in Invertase Activity and Changes in Carbohydrate Metabolism in Anthers.

This review discusses the role of abscisic acid (ABA)-based drought stress chemical signalling in regulating crop vegetative and reproductive development and its contributions to crop drought adaptation. Increased concentrations of ABA in the root induced by soil drying may maintain root growth and increase root hydraulic conductivity; both lead to an increase in water uptake and thereby postpone the development of water deficit in the shoot. Root ABA is also transported in the xylem to the shoot and is perceived at the acting sites, where it causes stomatal closure and reduced leaf expansion, thereby preventing dehydration of leaf tissues and enhancing the chance for survival under prolonged drought. ABA-based chemical signalling can be amplified by several factors, particularly increased pH in the xylem/apoplast, which retains anionic ABA. Such an increase in xylem pH detected in field-grown maize might have been brought about by reduced nitrate uptake by plants during soil drying. In contrast, xylem sap alkalinisation was not found in soybeans, which depend on fixing nitrogen through their association with Rhizobium japonicum. Evidence has also shown that the xylem-borne ABA can be transported to plant reproductive structures and influence their development, presumably by regulating gene expression that controls cell division and carbohydrate metabolic enzyme activity under drought conditions. The possible involvement of ABA in the up- and down-regulation of acid invertase in crop source (adult leaves) v. sink (young ovaries) organs indicates a crucial role of the hormone in balancing source and sink relationship in plants according to the availability of water in the soil. A novel irrigation technique named partial root-zone drying (PRD), has been developed to allow exploitation of ABA-based drought stress signalling to improve water-use efficiency (WUE) based on its roles in regulating stomatal aperture and leaf expansion. However, little is known about how crop reproductive development is regulated when irrigated under PRD. We suggest that more attention should be paid to the latter aspect as it directly relates to crop yield and quality.

A review of drought adaptation in crop plants: changes in vegetative and reproductive physiology induced by ABA-based chemical signals

Using detached ears of wheat cultured in nutrient solution the effect of sucrose and ABA supply on grain number was examined. In ears detached prior to ear emergence, to correspond with the time of pollen mother cell meiosis, higher levels of sucrose uptake were associated with higher grain number per ear. ABA indirectly caused a reduction in grain number by decreasing uptake of sucrose through decreasing stomatal conductance and transpiration. There was possibly also a direct effect of ABA on grain number. At higher levels of ABA the negative effect on grain number was decreased by increasing the sucrose concentration. In ears detached one to three days after anthesis grain number was also influenced by the amount of sucrose taken up, although grain number was not as sensitive to the sucrose supply at this time as it was at meiosis. The influence of ABA following anthesis was limited to an indirect effect on grain number through reductions in sucrose uptake.

Stephen P. Waters

Papers

The Influence of Sucrose and Abscisic Acid on the Determination of Grain Number in Wheat