Single‐cell transcriptomic analysis of pea shoot development and cell‐type‐specific responses to boron deficiency

Abstract

SUMMARYUnderstanding how nutrient stress impacts plant growth is fundamentally important to the development of approaches to improve crop production under nutrient limitation. Here we applied single‐cell RNA sequencing to shoot apices of Pisum sativum grown under boron (B) deficiency. We identified up to 15 cell clusters based on the clustering of gene expression profiles and verified cell identity with cell‐type‐specific marker gene expression. Different cell types responded differently to B deficiency. Specifically, the expression of photosynthetic genes in mesophyll cells (MCs) was down‐regulated by B deficiency, consistent with impaired photosynthetic rate. Furthermore, the down‐regulation of stomatal development genes in guard cells, including homologs of MUTE and TOO MANY MOUTHS, correlated with a decrease in stomatal density under B deficiency. We also constructed the developmental trajectory of the shoot apical meristem (SAM) cells and a transcription factor interaction network. The developmental progression of SAM to MC was characterized by up‐regulation of genes encoding histones and chromatin assembly and remodeling proteins including homologs of FASCIATA1 (FAS1) and SWITCH DEFECTIVE/SUCROSE NON‐FERMENTABLE (SWI/SNF) complex. However, B deficiency suppressed their expression, which helps to explain impaired SAM development under B deficiency. These results represent a major advance over bulk‐tissue RNA‐seq analysis in which cell‐type‐specific responses are lost and hence important physiological responses to B deficiency are missed. The reported findings reveal strategies by which plants adapt to B deficiency thus offering breeders a set of specific targets for genetic improvement. The reported approach and resources have potential applications well beyond P. sativum species and could be applied to various legumes to improve their adaptability to multiple nutrient or abiotic stresses.

The Shoot Apical Meristem: An Evolutionary Molding of Higher Plants

“…The expression of these genes was suppressed, suggesting a reorganization of chromatin during SAM development and a possibly impaired SAM activity under B deficiency. These results emphasize the importance of considering cell type-specific stress responses, which may be key to unraveling complex biological processes [147].…”

“…Sc/snRNAseq offers the possibility to study division and differentiation at cell resolution, quantifying the contribution of individual cells during the formation of new aerial structures, a task that was impossible before this technology [15]. Currently, three SAM scRNA-seq studies in Arabidopsis [145], one in maize [146], and one in pea [147], and two SAM snRNA-seq studies, one in tomato [148] and one in Populus [149], are available (Table 1). The transcriptomic landscape of the Arabidopsis SAM is an invaluable reference due to its status as the most extensively studied plant model species and has led to numerous resources for single-cell analysis.…”

Linking the key physiological functions of essential micronutrients to their deficiency symptoms in plants

“…The arrest of meristematic activity occurs already within the first hour after B deprivation, as cells become unable to divide and elongate properly (Poza‐Viejo et al ., 2018). In shoots, growth and development are negatively affected by a range of processes, including downregulation of photosynthetic genes in the developing mesophyll cells and genes related to stomatal development and density (Chen et al ., 2023a). Boron deficiency also suppresses the expression of genes encoding histones and chromatin assembly and remodelling proteins, which further impairs the shoot apical meristem activity (Chen et al ., 2023a).…”

“…In shoots, growth and development are negatively affected by a range of processes, including downregulation of photosynthetic genes in the developing mesophyll cells and genes related to stomatal development and density (Chen et al ., 2023a). Boron deficiency also suppresses the expression of genes encoding histones and chromatin assembly and remodelling proteins, which further impairs the shoot apical meristem activity (Chen et al ., 2023a). In roots, the disorganization of the meristem results in a stubby, swollen appearance, frequently with increased root hair formation (Fig.…”

Genome-wide analysis of respiratory burst oxidase homolog gene family in pea (Pisum sativum L.)

“…As a classic model plant and the second most important grain legume, pea ( Pisum sativum L., 2n = 14) has been widely used in genetics and developmental biology studies since Mendel ( Kreplak et al., 2019 ; Chen et al., 2022 ; Chen et al., 2023 ; Li et al., 2023 ). Pea has become an important legume crop and green vegetable favored by many people worldwide.…”