Investigating the impact of mobile signals on potato development and productivity

Abstract

Plants grow in a highly dynamic and complex environment, where adaptability and plasticity are key factors for their survival and development. Mobile signals, whether short- or long-distance, play an essential role in enabling plants to optimize their growth, development, yield, and responses to environmental stresses. To better understand these processes, we conducted a comprehensive literature review summarizing three decades of research on long-distance signaling in plants. This review aimed to consolidate the current knowledge, identify gaps, and explore emerging directions in the field. Notably, several mobile signals have been identified in potato that are central to tuber development. These signals are diverse in nature—including mRNAs (e.g., BEL5, BEL11, BEL29), proteins (SP6A, SP3D), microRNAs (miR156, miR172), RNA-binding proteins (PTB1, PTB6), and sucrose. Under tuber-inductive conditions, these signals are selectively transported to the belowground stolons, where they initiate and promote tuber formation. However, it remains unclear whether these signals could act synergistically and influence potato development. To explore this, we employed a multi-gene stacking approach involving a key mobile RNA, StBEL5, along with its associated RNA-binding proteins, StPTB1 and StPTB6. This strategy was applied to two potato cultivars and led to early tuberization as well as a 2–4-fold increase in tuber yield. The expression patterns of key tuber marker genes were also consistent with the observed increase in productivity. This multi-gene stacking method could be applied to other crops where agronomic traits are influenced by mobile macromolecules, expanding the potential for improving crop traits. A stolon, under tuber-inductive conditions, typically develops into a tuber. Alternatively, exposure to light may induce the stolon to differentiate into a shoot. The HD-ZIP class III transcription factor family, regulated by miR165/166, is crucial in maintaining meristem activity. During early tuberization, we observed that miR166 is abundant in the stolons. In our study, suppressing miR166 in Solanum tuberosum ssp. andigena resulted in altered tuber morphology, including elongated and pigmented tubers under short-day conditions. These phenotypic changes were found to be associated with differential auxin accumulation and altered expression of auxin biosynthesis and transport genes in stolons. We further showed that the HD-ZIP class III transcription factor REVOLUTA affects the promoter activity of auxin biosynthesis genes in potato and may influence auxin dynamics during tuberization. In addition to systemic mobile signals, several developmental decisions appear to be locally regulated within the stolon tip. A stolon, being a modified stem, has the unique potential to develop into either a shoot or a tuber—a remarkable example of developmental plasticity. However, the molecular basis of this dual fate remains poorly understood. In our study, we characterized the stages of stolon differentiation and demonstrated that direct light perception by stolons promotes shoot formation. Moreover, stolons normally develop exclusively from belowground axillary meristems, unlike aerial ones. We propose that a complex interplay between light cues, hormone signaling pathways, and gene regulatory networks governs the initiation of stolons from belowground axillary meristems, and regulates their developmental plasticity, determining whether they differentiate into shoots or tubers.