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Mate choice in plants

Plants are very selective when it comes to choosing mates. Flowering plant pollination systems are clever devices for attracting pollinators like birds, ants, and insects, but there are also mechanisms for keeping out unwanted pollen. Some plants happily self-fertilize with their own pollen but others reject such pollen because of the deleterious effects of inbreeding. In these plants, their own pollen or that of close relatives is rejected if it lands on the female stigma. For all plants, the pollen of other species is undesirable, as it will result in aborted zygotes or infertile offspring. Plants have evolved various mechanisms for rejecting unwanted pollen. The self-incompatibility (SI) system, found in several plant families, including the Solanaceae, which includes tobacco, tomato, and eggplant, is the best studied. A number of components that function in the SI system have been identified, but the exact molecular mechanisms by which incompatible pollen is recognized and rejected and compatible pollen allowed to proceed to the ovary are still unknown. Understanding the molecular mechanisms of pollen recognition is important for designing novel plant breeding systems as well as ensuring safeguards against unwanted pollination by genetically modified crops.

Dr. Felipe Cruz Garca and his colleagues Karina Jimenez Duran, Grethel Busot, Claudia Ibarra Sanchez, and Bruce McClure have been investigating the components of the self-incompatibility system in tobacco. Dr. Cruz-Garcia, of the Departamento de Bioqumica, Facultad de Qumica, Universidad Nacional Autonoma de Mxico, will be presenting this work at a symposium on the Biology of Solanaceous Species at the annual meeting of the American Society of Plant Biologists in Mrida, Mexico (June 29, 11:00 AM).

In flowering plants, the female reproductive organ, the pistil, comprises the stigma, style, and ovary. The stigma catches pollen shed by the male anthers. If the pollen is compatible, it will germinate and send tubes through the extracellular matrix (ECM) of the style toward the ovary. It is in the style ECM where recognition and acceptance or rejection of the pollen takes place. Compatible pollen tubes grow unhindered toward the ovary. Incompatible pollen tubes become distorted and stop growing. The recognition mechanism is analogous to the immune systems in animals. Factors present in both the ECM and the pollen are needed for recognition and rejection or acceptance.

The most widespread SI system is genetically controlled at the chromosomal region called the S locus, which contains numerous alleles that control recognition specificity. These genes code for S-locus ribonucleases (S-RNases), enzymes that degrade RNA. S-RNases are expressed in the stigma, style and ovary and concentrate in the style ECM where they interact with pollen tubes. The recognition factors on the pollen side are the SLF (S-locus, F-box) alleles. If the S alleles of the pollen match those in the stylar ECM, the pollen is rejected. If they are different, the pollen tubes are allowed to grow toward the ovary.

The exact nature of the interactions is still unclear, but the work of Cruz-Garcia and other scientists suggests that S-RNases are taken up into the pollen tubes and sequestered there in vacuoles. If the pollen is too closely related and therefore incompatible, the vacuolar compartments are somehow disrupted, and the S-RNases released to the cytosol begin to destroy the RNA of the pollen tubes, in effect, killing them. However, S-specific matching between S-RNase and SLF, by itself is not sufficient for rejection of incompatible pollen. Other factors not linked to the S locus are also required in the genera Nicotiana (tobacco), Solanum (tomato) and Petunia. Three other glycoproteins, proteins with attached carbohydrate components, have been found to be associated with pollen tubes. These proteins, transmitting-tract-specific (TTS), 120 kDa glycoprotein (120K), and pistil extension-like protein III (PELPIII), may play a role in movement of S-RNases into the pollen tube vacuoles and, if necessary, into the pollen tube cytoplasm, where they destroy RNA.

Cruz-Garcia and his colleagues have been investigating the non-S-locus factors in the tobacco species Nicotiana alata. They have recently identified and characterized another factor, Stigma Expressed Protein (NaStEP) in N. alata. Sequencing revealed that it is homologous to proteinase inhibitors, enzymes that prevent protein degradation, and that it contains a sequence that targets it to the vacuoles of unpollinated stigmas. If incompatible pollen lands on these stigmas, NaStEP is released into the stigmatic exudates where it associates with pollen tubes. If the NaStEP gene is silenced, the SI rejection system breaks down, so NaStEP clearly plays a role in the pollen rejection mechanism.

Because of their immobility, plants face numerous challenges to ensure reproductive success and genetic diversity. Remarkably, they have evolved more than one system of mate choice, and components of the best studied are still being discovered. Knowledge of these systems may help us engineer plant breeding systems more precisely to achieve greater yields and to provide built-in safeguards for preventing inadvertent pollination by and in pest or insecticide resistant crops or those bred to produce drugs or industrial materials.


Contact: Dr. Felipe Cruz-Garcia
American Society of Plant Biologists

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