The central role of stem cells in determining plant longevity variation

Abstract

Vascular plants display a huge variety of longevity patterns, from a few weeks for several annual species up to thousands of years for some perennial species. Understanding how longevity variation is structured has long been considered a fundamental aspect of the life sciences in view of evolution, species distribution, and adaptation to diverse environments. Unlike animals, whose organs are typically formed during embryogenesis, vascular plants manage to extend their life by continuously producing new tissues and organs in apical and lateral directions via proliferation of stem cells located within specialized tissues called meristems. Stem cells are the main source of plant longevity. Variation in plant longevity is highly dependent on the activity and fate identity of stem cells. Multiple developmental factors determine how stem cells contribute to variation in plant longevity. In this review, we provide an overview of the genetic mechanisms, hormonal signaling, and environmental factors involved in controlling plant longevity through long-term maintenance of stem cell fate identity.

Keywords: annual plants; axillary meristems; perennial plants; plant longevity; stem cells.

Figure 1

Stem cells in plants. (A) Schematic of a longitudinal section of the shoot apical meristem (SAM) in Arabidopsis. The SAM consists of three developmental zones: (i) the central zone (CZ; red) with a population of slowly dividing stem cells; (ii) the surrounding peripheral zone (yellow), where cells divide rapidly to give rise to lateral organs; and (iii) the rib zone (green), where cells differentiate into central stem tissue. (B) Schematic of a longitudinal section of the root apical meristem (RAM) in Arabidopsis. The RAM consists of a small group of cells that form the quiescent center (QC; blue) and is surrounded by stem cells (red). Signals from the QC maintain the stem cell niche of the surrounding stem cells. (C) Schematic of a cross-section through the Arabidopsis inflorescence stem. The vascular cambium meristem (VCM) is shown in red. The vascular cambium generates the xylem (yellow) and phloem (blue) by inward and outward cell division, respectively.

Figure 2

Molecular regulation of developmental phase transitions in Arabidopsis. (A) The juvenile-to-adult phase transition is regulated by miR156/157 (master regulator) and AHLs through repression of SPL gene expression. The age-related downregulation of miR156/157 and AHLs leads to enhanced production of SPL proteins, which promotes adult leaf morphology. The level of miR172 increases markedly through the activity of SPLs. Increased levels of miR172 suppress production of the TOE1 and TOE2 transcription factors, thereby allowing development of trichomes on the abaxial side of leaves. SPL abundance promotes the juvenile-to-adult phase transition in part by downregulating AHLs. Arrows and blunted lines indicate positive and negative regulation of the target activity, respectively. (B) A simplified model of the photoperiod-, vernalization-, age-, and gibberellic acid (GA)-dependent pathways of flowering regulation in Arabidopsis. In the photoperiod pathway, light signaling leads to CO accumulation in leaves, where CO directly activates expression of the FT gene. FT is a florigen protein that moves through the phloem to the SAM and triggers flowering by interacting with FD and activating SOC1 and, as a result, AP1 and LFY. In the vernalization pathway, flowering time is determined by long-term cold that leads to epigenetic silencing of the FLC gene. The MADS-box protein FLC represses flowering mainly by downregulating flowering-time integrators, including FT, FD, and SOC1. In the age-dependent pathway, a gradual decline in miR156/157 level with plant age allows SPL abundance to increase, thereby activating SOC1 and other floral integrators (not shown). Finally, GA signaling is an independent pathway that regulates flowering by activation of the SOC1 and SPL genes. Subsequently, all four pathways help with transcriptional regulation of the floral integrators FT and SOC1, which promote AP1 and LFY expression. AP1 and LFY are necessary to complete the floral transition. Arrows and blunted lines indicate positive and negative regulation of the target activity, respectively. Created with BioRender.

Figure 3

Developmental phase identity of AMs. (A and B) Schematic of the GRN that mediates the immediate development of AMs into inflorescences in Arabidopsis accession Col-0 (A) or extends vegetative identity to result in an increased number of rosette leaves on basal nodes and aerial rosettes in accession Sy-0 (B). Blunt-ended lines indicate repression, and arrows indicate promotion. Black indicates genes that are expressed; gray represents repressed genes.