The evolutionary conversion of leaves to spines in cacti
One defining feature of cacti is having clusters of spines. Numerous plants have spines of course, but in cacti, spines occur in clusters in the axil of leaves, even though the leaves are usually microscopic. Most cactus morphologists have concluded that cactus spines are either modified leaves or modified bud scales (the difference is inconsequential because bud scales themselves are modified leaves). The leaf-nature of spines is certainly understandable from the point of view of location: spine primordia look just like leaf primordia and are produced at a location where we would expect leaf primordia at the base of the axillary buds shoot apical meristem.
Evolution appears to have been more complex than would be expected: mature cactus spines do not contain any of the cells or tissues characteristic of leaves, and conversely leaves lack all features characteristic of spines. The two organs have little in common other than developing from leaf primordia. Spines consist of just a core of fibers surrounded by sclereid-like epidermis cells. They have no stomata, no guard cells, no mesophyll parenchyma, no xylem, no phloem. When mature, all cells in a spine are dead, and even when the spine is still growing it has living cells only at its base. Cactus leaves on the other hand even the microscopic leaves of Cactoideae have parenchymatous epidermis cells, guard cells, spongy mesophyll, chlorenchyma, xylem and phloem. So the evolutionary conversion of cactus leaves into spines did not involve a mere reduction of the lamina and then further reduction of midrib and petiole, it instead involved the suppression of all leaf-cell type genes and activation of genes that control formation of fibers, the deposition and lignification of secondary walls, and then programmed cell death. These fiber morphogenesis genes are not activated in any cactus leaf (none at all has fibers), but they are activated of course in the development of wood. It would appear that after an axillary bud apical meristem initiates spine primordia, most leaf genes remain suppressed and instead wood fiber genes are activated. This does not involve all wood genes because vessels are never produced in the spines, just wood fibers. This would be a type of homeotic evolution.
A puzzling aspect of spine development is the phyllotactic arrangement of spine primordia around the axillary bud apical meristem. To be truly leaf-like, spine primordia should occur at the points of intersection of two sets of Fibonacci spirals centered on the axillary bud apical meristem just as ordinary leaves occur at the intersection points of spirals centered on the shoot apical meristem. But many spines occur in two rows, or all spine primordia occur on one side of the apical meristem but not on the other two or three sides. This was studied by Norman Boke who concluded that spine primordia do indeed arise in normal phyllotaxy, it is just that parts of the axillary bud are so crowded that the spine primordia in those areas are suppressed. Perhaps so, but further study is warranted. Boke also noticed that very often spine primordia that were the last to be initiated were the first to develop: primordium initiation was centripetal, maturation was centrifugal. This does not happen with leaves: the first leaf primordia to be initiated are the first to develop.
Spines that act as extra-floral nectaries in cacti
Other aspects of spine biology are complex and in need of study. In several genera, some spines in each axillary bud develop as glands, known as extrafloral nectaries. They secrete a sugar solution that attract ants. These spines consist of loosely arranged parenchyma cells that secrete into intercellular spaces, and the accumulating nectar is then forced upward and out through small holes in the epidermis. Such spines are short and broad but still have a spine-like organization with the secretory cells looking like short, broad, thin-walled fibers.
Mauseth, J. D. 1982. Development and ultrastructure of extrafloral nectaries in Ancistrocactus scheeri (Cactaceae). Botanical Gazette 143: 273 277.
Spines that provide shade in addition to (or instead of) protection
Many cacti are protected from full sunlight by a dense covering of spines. Rather surprisingly, perhaps as many as half of all cactus species are adapted to dark rainforests (Epiphyllum, Rhipsalis) or semi-shady shrublands/grasslands (Echinopsis, Mammillaria, Notocactus) or cool, wet, cloudy highlands (Austrocylindropuntia, Oroya, Soehrensia) (Habitats are described in Cactus Odyssey). Such plants would be killed quickly by exposure to full sunlight in Phoenix, Arizona. Species in such cool or semi-shady habitats often have either just a few spines or only very short ones. However, cacti from intensely sunny, hot deserts often must have a complete covering of spines. In many cases, the spines are so strong and painful that they obviously offer both protection and shade, but in many species the spines are so soft that a hungry, thirsty animal would chew through them with no trouble. The benefit of such spines definitely appears to be blocking sunlight and thus preventing the plant from over heating, the chlorophyll from being bleached and the plant's DNA from being damaged. For example, in Mammillaria plumosa, spine epidermis cells project outward as long trichomes, giving the spine a feathery appearance. In other species, the spines are flat, thin and papery, being too flexible to deter animals, but broad enough to shade the plant (as well as to camouflage the cacti among the grasses with which it grows).
Mauseth, J. D., and W. Halperin. 1975. Hormonal control of organogenesis in Opuntia polyacantha (Cactaceae). American Journal of Botany 62: 869 877.
Mauseth, J. D. 1976. Cytokinin‑ and gibberellic acid‑induced effects on the structure and metabolism of shoot apical meristems in Opuntia polyacantha (Cactaceae). American Journal of Botany 63: 1295 1301.
Mauseth, J. D. 1977. Cytokinin‑ and gibberellic acid‑induced effects on the determination and morphogenesis of leaf primordia in Opuntia polyacantha (Cactaceae). American Journal of Botany 64: 337 346.
Mauseth, J. D., and C. Ostolaza. 2002. Parkas? Ice picks? Oxygen bottles? A cactus expedition in highland Peru. Part 1. The Cactus and Succulent Journal (USA) 74: 52 63.
Part 2. The Cactus and Succulent Journal (USA) 74: 127 133.
Part 3. The Cactus and Succulent Journal (USA) 74: 212 215.