Single-cell transcriptomics reveal heterogeneity in plant responses to the environment: a focus on biotic and abiotic interactions.

Environmental cues, from biotic or abiotic origin, are major factors influencing plant growth and productivity. Interactions with biotic (e.g. symbionts and pathogens) and abiotic (e.g. changes in temperature, water or nutrient availability) factors trigger signaling and downstream transcriptome changes in plants. While bulk RNA-sequencing technologies have traditionally been used to profile these transcriptional changes, the heterogeneity of the responses, caused by the cellular complexity of organs, might be masked by homogenizing tissues. Thus, whether different cell types respond equally to environmental fluctuations, or whether subsets of the responses are cell-type specific, are long-lasting questions in plant biology. The recent break-through of single-cell transcriptomics in plant research offers an unprecedented view on cellular responses under changing environmental conditions. In this review, we discuss the contributions of single-cell transcriptomics towards the understanding of cell-type specific plant responses to biotic and abiotic environmental interactions. Besides major biological findings, we present some technical challenges coupled to single-cell studies of plant-environment interactions, proposing possible solutions and exciting paths for future research.

SIAMESE-RELATED1 imposes differentiation of stomatal lineage ground cells into pavement cells.

The leaf epidermis represents a multifunctional tissue consisting of trichomes, pavement cells and stomata, the specialized cellular pores of the leaf. Pavement cells and stomata both originate from regulated divisions of stomatal lineage ground cells (SLGCs), but whereas the ontogeny of the stomata is well characterized, the genetic pathways activating pavement cell differentiation remain relatively unexplored. Here, we reveal that the cell cycle inhibitor SIAMESE-RELATED1 (SMR1) is essential for timely differentiation of SLGCs into pavement cells by terminating SLGC self-renewal potency, which depends on CYCLIN A proteins and CYCLIN-DEPENDENT KINASE B1. By controlling SLGC-to-pavement cell differentiation, SMR1 determines the ratio of pavement cells to stomata and adjusts epidermal development to suit environmental conditions. We therefore propose SMR1 as an attractive target for engineering climate-resilient plants.

Single-cell transcriptomics sheds light on the identity and metabolism of developing leaf cells.

As the main photosynthetic instruments of vascular plants, leaves are crucial and complex plant organs. A strict organization of leaf mesophyll and epidermal cell layers orchestrates photosynthesis and gas exchange. In addition, water and nutrients for leaf growth are transported through the vascular tissue. To establish the single-cell transcriptomic landscape of these different leaf tissues, we performed high-throughput transcriptome sequencing of individual cells isolated from young leaves of Arabidopsis (Arabidopsis thaliana) seedlings grown in two different environmental conditions. The detection of approximately 19,000 different transcripts in over 1,800 high-quality leaf cells revealed 14 cell populations composing the young, differentiating leaf. Besides the cell populations comprising the core leaf tissues, we identified subpopulations with a distinct identity or metabolic activity. In addition, we proposed cell-type-specific markers for each of these populations. Finally, an intuitive web tool allows for browsing the presented dataset. Our data present insights on how the different cell populations constituting a developing leaf are connected via developmental, metabolic, or stress-related trajectories.

Increasing yield on dry fields: molecular pathways with growing potential.

Drought stress constitutes one of the major constraints to agriculture all over the world, and its devastating effect is only expected to increase in the following years due to climate change. Concurrently, the increasing food demand in a steadily growing population requires a proportional increase in yield and crop production. In the past, research aimed to increase plant resilience to severe drought stress. However, this often resulted in stunted growth and reduced yield under favorable conditions or moderate drought. Nowadays, drought tolerance research aims to maintain plant growth and yield under drought conditions. Overall, recently deployed strategies to engineer drought tolerance in the lab can be classified into a 'growth-centered' strategy, which focuses on keeping growth unaffected by the drought stress, and a 'drought resilience without growth penalty' strategy, in which the main aim is still to boost drought resilience, while limiting the side effects on plant growth. In this review, we put the scope on these two strategies and some molecular players that were successfully engineered to generate drought-tolerant plants: abscisic acid, brassinosteroids, cytokinins, ethylene, ROS scavenging genes, strigolactones, and aquaporins. We discuss how these pathways participate in growth and stress response regulation under drought. Finally, we present an overview of the current insights and future perspectives in the development of new strategies to improve drought tolerance in the field.

Identification of Two Auxin-Regulated Potassium Transporters Involved in Seed Maturation.

The seed is the most important plant reproductive unit responsible for the evolutionary success of flowering plants. Aside from its essential function in the sexual reproduction of plants, the seed also represents the most economically important agricultural product worldwide, providing energy, nutrients, and raw materials for human nutrition, livestock feed, and countless manufactured goods. Hence, improvements in seed quality or size are highly valuable, due to their economic potential in agriculture. Recently, the importance of indolic compounds in regulating these traits has been reported for Arabidopsis thaliana. The transcriptional and physiological mechanisms involved, however, remain largely undisclosed. Potassium transporters have been suggested as possible mediators of embryo cell size, controlling turgor pressure during seed maturation. In addition, it has been demonstrated that the expression of K⁺ transporters is effectively regulated by auxin. Here, we provide evidence for the identification of two Arabidopsis K⁺ transporters, HAK/KT12 (At1g60160) and KUP4 (At4g23640), that are likely to be implicated in determining seed size during seed maturation and, at the same time, show a differential regulation by indole-3-acetic acid and indole-3-acetamide.