Characterization of Transcriptome Remodeling during Cambium Formation Identifies MOL1 and RUL1 As Opposing Regulators of Secondary Growth

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Abstract
Cell-to-cell communication is crucial for the development of multicellular organisms, especially during the generation of new tissues and organs. Secondary growth—the lateral expansion of plant growth axes—is a highly dynamic process that depends on the activity of the cambium. The cambium is a stem cell–like tissue whose activity is responsible for wood production and, thus, for the establishment of extended shoot and root systems. Attempts to study cambium regulation at the molecular level have been hampered by the limitations of performing genetic analyses in trees and by the difficulty of accessing this tissue in model systems such as Arabidopsis thaliana. Here, we describe the roles of two receptor-like kinases, REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1), as opposing regulators of cambium activity. Their identification was facilitated by a novel in vitro system in which cambium formation is induced in isolated Arabidopsis stem fragments. By combining this system with laser capture microdissection, we characterized transcriptome remodeling in a tissue- and stage-specific manner and identified series of genes induced during different phases of cambium formation. In summary, we provide a means for investigating cambium regulation in unprecedented depth and present two signaling components that control a process responsible for the accumulation of a large proportion of terrestrial biomass. In contrast to animals, plants have the capacity to grow and form new organs throughout their entire life cycle, thereby building up some of the largest organisms on earth. This remarkable capacity is based on the activity of stem cell–like tissues—the meristems—located at shoot and root apices and, in a large repertoire of species, in lateral positions at the flanks of growth axes. In comparison to apical meristems, our knowledge of the molecular mechanisms controlling the activity of lateral meristems like the cambium is very limited. This is despite the fact that lateral growth is responsible for wood formation, and thus for the accumulation of large amounts of terrestrial biomass, and for fixation of atmospheric CO2. Here, we introduce an in vitro system by which cambium initiation can be stimulated under controlled conditions in stems of the reference plant Arabidopsis thaliana. By revealing genome-wide and tissue-specific alterations in transcript accumulation during cambium initiation, we identify two novel receptor-like kinases, namely MOL1 and RUL1, as opposing cambium regulators. These findings demonstrate that our in vitro system represents a valuable tool for studying cambium regulation and open up possibilities to dissect lateral growth in plants from novel perspectives.