It is well described1
that under stress conditions many plant species accumulate proline as an adaptive response to adverse conditions. Although a clear-cut relationship between proline accumulation and stress adaptation has been questioned by some authors,2
it is generally believed that the increase in proline content following stress injury is beneficial for the plant cell.
However, ever since the early 80s different research groups found a significant amount of proline in the reproductive organs of different plant species, raising the possibility that the accumulation of this amino acid may also occur in physiological non-stressed conditions for developmental purposes. Chiang and Dandekar,3
for example, reported that in Arabidopsis reproductive tissues, such as florets, pollen, siliques and seeds, proline represents up to 26% of the total amino acid pool, while in vegetative tissues it only accounts for 1–3%. Even more striking, Schwacke et al.4
observed that the content of free proline in tomato flowers was 60-fold higher than in any other organ analyzed. Similar physiological accumulations of proline have been reported, at different concentrations, in reproductive organs of other plant species,3
and in most cases the overall levels of this amino acid seem too high to be accounted for only by an increased demand of protein synthesis.
At the molecular level, the differential accumulation of proline in reproductive tissues is thought to be primarily determined by upregulation of proline synthesis and transport genes, as upregulation of Δ1-pyrroline-5-carboxylate synthetase
), a gene encoding the rate-limiting enzyme of proline synthesis from glutamate, and Proline transporter T
), a gene encoding a specific proline transporter, has been found in flower organs.4–6
The role exerted by the proline catabolic genes in the process of developmental proline accumulation, in contrast, appear different from the role played by these genes during stress-induced proline accumulation, as proline dehydrogenase
) and Δ1-pyrroline-5-carboxylate dehydrogenase
) catabolic genes are upregulated in the former case,7–9
and downregulated in the latter case.8,10
Although the developmental accumulation of proline in reproductive organs has been repeatedly reported, and seems to be a widespread phenomenon among plant species, its functional meaning is still matter of debate. An obvious function of proline in development may be the protection of developing cells from osmotic damages, especially in those developmental processes, such as pollen development and embryogenesis, in which tissues undergo spontaneous dehydratation. Similarly to the osmotic stress caused by environmental factors, the desiccation process that spontaneously occurs in reproductive tissues may seriously damage the plant cell, and it is likely to be counteracted by proline accumulation. Accordingly, higher levels of proline have been measured3
in tissues with low water content as compared as to tissues with high water content. The correlation between proline accumulation and water content, however, is not very tight. Florets, for example, have been described by Chiang and colleagues as the organs with the highest proline concentration, in spite of their relatively high water content.
As an alternative possibility, proline has been proposed to provide energy to sustain metabolically demanding programs of plant reproduction. In a similar way, proline is used in animal systems to fuel the initial phase—the most energy—dependent—of the flight of many insects, such as bees and butterflies.11
Since the oxidation of one molecule of proline yields 30 ATP equivalents,12
this amino acid seems well suited to sustain high energy-requiring processes. The upregulation of the proline catabolic genes typically observed in flowers, siliques and seeds is consistent with the need to provide the plant with energy throughout the whole reproductive phase.