From morphological modules to lineage-derived subindividuals: integrating phenotypic, epigenetic and genetic...

Harper's (1977) framing of the plant as a population of semi-autonomous modules remains foundational but predates genomic tools able to test the genetic identity of individual modules. Two further literatures address within-plant heterogeneity largely in parallel: a genetic-mosaicism literature (Gill et al., 1995; Reusch et al., 2021) showing that somatic mutations accumulate within plants, and a subindividual-variation literature (Herrera, 2009; Sobral and Sampedro, 2022) documenting functional consequences of within-plant phenotypic and epigenetic diversity.

We bridge these bodies of work within a single lineage-based framework. We define a plant subindividual as a cell-lineage-derived module with a traceable developmental history and partial autonomy, whose differentiation may be expressed at phenotypic, epigenetic and/or genetic levels; detectable somatic genetic divergence is not required for subindividual status. Drawing on whole-genome and methylome studies of long-lived trees, shrubs and clonal crops, we assess the strength of support at each level, distinguishing evidence for the existence of within-plant heterogeneity from evidence for its effects on module function. In the studies reviewed here, a causal link between somatic variants in signalling genes and module-specific physiological responses remains to be established. We then propose a distinct scaling hypothesis: for responses requiring rapid or pathway-specific signalling, increasing transport distance and vascular sectoriality may raise the relative contribution of local regulation-a testable account of why module autonomy may scale with plant size.

Reframing plant modules as lineage-derived subindividuals yields testable predictions comparing genetic, epigenetic and phenotypic differentiation across life histories-from mainly phenotypic and epigenetic differentiation in short-lived herbs to detectable genetic mosaicism in long-lived trees and clonal crops. The framework connects three lines of research and proposes a testable scaling hypothesis for module autonomy.