Moderately elevated temperature stress (METS) did not affect vegetative growth () or reproductive development such as the number of flowers () and the number of pollen grains produced (), but significantly reduced the number of fruit set (). The reduction of fruit set under the stress was likely to be caused by reduction in pollen viability () and release (); this agrees with previous reports (Sato et al., 2000
) in which plants were grown under artificial light conditions. Photosynthetic ability under high temperature stress has been a major research topic in various agricultural crops, including tomatoes (Bar-Tsur et al., 1985
; Camejo et al., 2005
; Nautiyal et al., 2005
). However, this experiment, conducted under natural light condition with the same temperature regimes as in the previous report of Sato et al. (2005)
, indicates that the source strength such as photosynthetic ability is not a major limiting factor of tomato fruit set under moderately elevated temperature stress regardless of the light conditions. Carbon dioxide (CO2
) is one of the major sources of global warming. It is known that higher CO2
concentration enhances growth rate in various plants (Pooter et al
., 1996). The present results, however, imply that the productivity of grain crops and fruit vegetables might not be enhanced by high CO2
since reproductive development is much more sensitive even to a moderate increase in temperature.
In the present experiment, tomato fruit set correlated with pollen grain viability and pollen release (). Pollen grains need to accumulate enough reserve to be viable. A major form of reserve in mature pollen grains of tomato is starch (Polowich and Sawhney, 1993). Prior to starch accumulation, sucrose, a major form of carbohydrate transport in tomato, must be transferred from source organs (i.e. photosynthetically active leaves) to sink organs (i.e. flowers, or more specifically anthers) via phloem. After sucrose is transported, and prior to starch synthesis, sucrose is hydrolysed by invertase to produce hexoses, because a basic component of starch is the α-1,4 linkage of glucose. Several isoforms of invertase have been isolated in various plants, including one uniquely expressed in tomato fruit vascular tissue (GenBank accession number Z12027). The present analysis indicated that tomato plants grown at METS had lower hexose (glucose and fructose) content in stamens at immature microspore and mature pollen grain stages (), but higher sucrose content (). Furthermore, the copy number of acid invertase mRNA tended to be lower in METS than CONT throughout the investigation (). Therefore, it seems that METS did not affect carbohydrate transport from the source to the anther, but disrupted sucrose hydrolysis and prevented normal pollen development, leading to the loss of pollen viability and the reduction in fruit set.
Disturbed sugar metabolism might have affected anther development as observed (); the length of stamen was approx. 26
% reduced in METS when compared with CONT. As a result of reduced anther growth, the stigma protruded out of the anther cone (). Such a phenomenon is often observed in summer tomato production and has been known as ‘stigma elongation’. The present results, however, indicate that the phenomenon is ‘anther shortening’ rather than stigma elongation.
Proline has been reported as one of the factors affecting pollen viability (Zhang and Croes, 1983
; Lansac et al., 1996
). In tomato, proline concentration in reproductive organs was found to be six to ten times higher than in the rest of the plant (Schwacke et al., 1999
). In the present experiment, proline content in anthers did not change between the treatments, except in the meiosis stage. Since a developing anther is a sink organ, most amino acids, including proline, are transported from source organs—as discussed on sucrose above. Sink–source translocation requires trafficking between symplastic and apoplastic environments and vice versa
, because nutrients produced in the symplast of source tissues (i.e. most likely the photosynthetic leaves) have to cross a plasma membrane for translocation via phloem. After translocation to sink organs (i.e. developing flower buds, anther and microspores), nutrients move to a symplastic environment, because most nutrients supplied to developing microspores will be carried out through tapetum cells. Tapetum is a cell layer which takes a crucial role in supplying nutritional storage during pollen development and degrades around the time of pollen mitosis in a programmed cell death fashion (Scott et al., 2004
). Prior to and during degradation, tapetum cells supply various nutrients such as amino acids, lipids and carbohydrate. Therefore, proline has to pass a plasma membrane at least a few times before reaching pollen grains. In the current experiment, it was observed that the proline content of the anthers was not significantly different between CONT and METS, except at the meiosis stage (). The copy number of proline transporter 1, which is expressed specifically at the pollen surface (Schwacke et al., 1999
), was significantly lower in METS at meiosis and mature pollen grain stages (). Therefore, it is reasonable to conclude that the disruption of proline transport into the developing pollen grain is part of the reason for the loss of pollen viability under METS.
Tapetum cell development and degradation should be precisely orchestrated with pollen development (Twell, 2002
) and any alteration in initiation and/or duration of tapetum degradation should influence pollen development. Evidence that a large number of male sterile mutants are related with defects of tapetum cell differentiation (Kaul, 1988
; Van der Meer et al., 1992
; Chaudhury, 1993
; Aarts et al., 1997
; Taylor et al., 1998
; Sanders et al., 1999
) may suggest the impairment of tapetum degradation could participate in the loss of pollen viability which caused fruit set reduction under METS. In heat shock research, Iwahori (1965)
reported that tomato plants subjected to 40
°C for 3
h for two consecutive days did not have tapetum degradation but indicated the loss of pollen viability. Under METS, however, tapetum degradation still occurred, although it was delayed. Therefore, the impact of moderately elevated temperature stress on plant reproduction differs from the impact of heat shock, or acute high temperature stress.
In the present experiment, a possible consequence of global warming to agricultural production has been presented and explained at a physiological and molecular level; moderate increases of atmospheric average temperature are likely to cause a significant reduction in tomato fruit set, which can be attributed to the disruption of specific physiological and molecular events during the narrow window of male reproductive development.