The Evolution of Growth Forms with Expanded Root and Shoot Parenchymatous Storage Is Correlated across the Eudicots

Premise of research. Plant succulence in leaves, stems, hypocotyls, and roots is heralded as an adaptation to aridity. Subterranean succulence is an underappreciated dimension of succulent plant diversity. Remarkable parallel evolution of proliferation of parenchyma and vascularization of stem and root parenchyma reported in previous case studies led us to predict that the evolution of stem succulence is tightly coupled to the evolution of subterranean succulence more broadly across the eudicots. Methodology. We applied a taxonomic rank-based measurement of relatedness to examine the distances between eudicot taxa with aboveground succulence (representing >20 separate origins of succulence) and their closest relatives with subterranean succulence. We compared these distances to the distances between a random sample of eudicot taxa that lack aboveground succulence (mesophytes) and their closest relatives with subterranean succulence. Pivotal results. Using a statistically conservative test, the ancestral distance test, we found that taxa with aboveground succulence were significantly more closely related to taxa with subterranean succulence than are mesophytes. Strikingly, all groups in which extensive aboveground succulence evolved are closely related to taxa with subterranean succulence, with the exception of the Fouquieriaceae. Conclusions. The phylogenetic coupling between aboveground and belowground succulence is a broad and strong pattern across a huge clade of plants, the eudicots. Despite high relatedness among taxa with aboveground and belowground succulence, the adaptive benefits of parenchymatous tissue are complex, and they likely differ for aboveground and belowground plant organs. The apparent lability of evolutionary change among succulent forms may reflect a common developmental program for parenchyma production whose spatial expression in different plant organs is altered during evolutionary diversification. These results encourage an expanded view of the evolutionary convergence among succulent plant forms that includes both aboveground and belowground components.