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ABSTRACT Plant immunity activation often results in suppression of plant growth, particularly in the case of constitutive immune activation. We discovered that signaling of the phytohormone cytokinin (CK), known to regulate plant growth through the control of cell division and shoot apical meristem (SAM) activity, can be suppressed by negative crosstalk with the defense phytohormones jasmonic acid (JA), and most evidently, salicylic acid (SA). We show that changing the negative crosstalk of SA on CK signaling in autoimmunity mutants by targeted increase of endogenous CK levels results in plants resistant to pathogens from diverse lifestyles, and relieves suppression of reproductive growth. Moreover, such changes in crosstalk result in a novel reproductive growth phenotype, suggesting a role for defense phytohormones in the SAM, likely through regulation of nitrogen response and cellular redox status. Our data suggest that targeted phytohormone crosstalk engineering can be used to achieve increased reproductive growth and pathogen resistance. SIGNIFICANCE STATEMENTPlants constantly integrate environmental stimuli with developmental programs to optimize their growth and fitness. Excessive activation of the plant immune system often leads to decreased plant growth, a process known as the growth-defense tradeoff. Here, we adapted phytohormone levels in Arabidopsis reproductive tissues of autoimmunity mutants to change phytohormonal crosstalk and diminish the growth tradeoff, resulting in increased broad resistance to pathogens and decreased growth suppression. Similar approaches to phytohormone crosstalk engineering could be used in different contexts to achieve outcomes of higher plant stress resilience and yield. 

SUMMARY Stem cells in plant shoots are a rare population of cells that produce leaves, fruits and seeds, vital sources for food and bioethanol. Uncovering regulators expressed in these stem cells will inform crop engineering to boost productivity. Single-cell analysis is a powerful tool for identifying regulators expressed in specific groups of cells. However, accessing plant shoot stem cells is challenging. Recent single-cell analyses of plant shoots have not captured these cells, and failed to detect stem cell regulators likeCLAVATA3andWUSCHEL. In this study, we finely dissected stem cell-enriched shoot tissues from both maize and arabidopsis for single-cell RNA-seq profiling. We optimized protocols to efficiently recover thousands ofCLAVATA3andWUSCHELexpressed cells. A cross-species comparison identified conserved stem cell regulators between maize and arabidopsis. We also performed single-cell RNA-seq on maize stem cell overproliferation mutants to find additional candidate regulators. Expression of candidate stem cell genes was validated using spatial transcriptomics, and we functionally confirmed roles in shoot development. These candidates include a family of ribosome-associated RNA-binding proteins, and two families of sugar kinase genes related to hypoxia signaling and cytokinin hormone homeostasis. These large-scale single-cell profiling of stem cells provide a resource for mining stem cell regulators, which show significant association with yield traits. Overall, our discoveries advance the understanding of shoot development and open avenues for manipulating diverse crops to enhance food and energy security.