Glucose produced from photosynthesis is a key nutrient signal regulating root meristem activity in plants; however, the underlying mechanisms remain poorly understood. Here, we show that, by modulating reactive oxygen species (ROS) levels, the conserved macroautophagy/autophagy degradation pathway contributes to glucose-regulated root meristem maintenance. In Arabidopsis thaliana roots, a short exposure to elevated glucose temporarily suppresses constitutive autophagosome formation. The autophagy-defective autophagy-related gene (atg) mutants have enhanced tolerance to glucose, established downstream of the glucose sensors, and accumulate less glucose-induced ROS in the root tips. Moreover, the enhanced root meristem activities in the atg mutants are associated with improved auxin gradients and auxin responses. By acting with AT4G39850/ABCD1 (ATP-binding cassette D1; Formerly PXA1/peroxisomal ABC transporter 1), autophagy plays an indispensable role in the glucose-promoted degradation of root peroxisomes, and the atg mutant phenotype is partially rescued by the overexpression of ABCD1. Together, our findings suggest that autophagy is an essential mechanism for glucose-mediated maintenance of the root meristem. Abbreviation: ABA: abscisic acid; ABCD1: ATP-binding cassette D1; ABO: ABA overly sensitive; AsA: ascorbic acid; ATG: autophagy related; CFP: cyan fluorescent protein; Co-IP: co-immunoprecipitation; DAB: 3’,3’-diaininobenzidine; DCFH-DA: 2’,7’-dichlorodihydrofluorescin diacetate; DR5: a synthetic auxin response element consists of tandem direct repeats of 11 bp that included the auxin-responsive TGTCTC element; DZ: differentiation zone; EZ, elongation zone; GFP, green fluorescent protein; GSH, glutathione; GUS: β-glucuronidase; HXK1: hexokinase 1; H₂O₂: hydrogen peroxide; IAA: indole-3-acetic acid; IBA: indole-3-butyric acid; KIN10/11: SNF1 kinase homolog 10/11; MDC: monodansylcadaverine; MS: Murashige and Skoog; MZ: meristem zone; NBT: nitroblue tetrazolium; NPA: 1-N-naphtylphthalamic acid; OxIAA: 2-oxindole-3-acetic acid; PIN: PIN-FORMED; PLT: PLETHORA; QC: quiescent center; RGS1: Regulator of G-protein signaling 1; ROS: reactive oxygen species; SCR: SCARECROW; SHR, SHORT-ROOT; SKL: Ser-Lys-Leu; SnRK1: SNF1-related kinase 1; TOR: target of rapamycin; UPB1: UPBEAT1; WOX5: WUSCHEL related homeobox 5; Y2H: yeast two-hybrid; YFP: yellow fluorescent protein

Summary: Rice is a staple food crop worldwide, and its production is severely threatened by phloem‐feeding insect herbivores, particularly the brown planthopper (BPH, Nilaparvata lugens), and destructive pathogens. Despite the identification of many BPH resistance genes, the molecular basis of rice resistance to BPH remains largely unclear. Here, we report that the plant elicitor peptide (Pep) signalling confers rice resistance to BPH. Both rice PEP RECEPTORs (PEPRs) and PRECURSORs of PEP (PROPEPs), particularly OsPROPEP3, were transcriptionally induced in leaf sheaths upon BPH infestation. Knockout of OsPEPRs impaired rice resistance to BPH, whereas exogenous application of OsPep3 improved the resistance. Hormone measurement and co‐profiling of transcriptomics and metabolomics in OsPep3‐treated rice leaf sheaths suggested potential contributions of jasmonic acid biosynthesis, lipid metabolism and phenylpropanoid metabolism to OsPep3‐induced rice immunity. Moreover, OsPep3 elicitation also strengthened rice resistance to the fungal pathogen Magnaporthe oryzae and bacterial pathogen Xanthamonas oryzae pv. oryzae and provoked immune responses in wheat. Collectively, this work demonstrates a previously unappreciated importance of the Pep signalling in plants for combating piercing‐sucking insect herbivores and promises exogenous application of OsPep3 as an eco‐friendly immune stimulator in agriculture for crop protection against a broad spectrum of insect pests and pathogens.

Multidrug and Toxic Compound Extrusion (MATE) proteins are essential transporters that extrude metabolites and participate in plant development and the detoxification of toxins. Little is known about the MATE gene family in the Solanaceae, which includes species that produce a broad range of specialized metabolites. Here, we identified and analyzed the complement of MATE genes in pepper (Capsicum annuum) and potato (Solanum tuberosum). We classified all MATE genes into five groups based on their phylogenetic relationships and their gene and protein structures. Moreover, we discovered that tandem duplication contributed significantly to the expansion of the pepper MATE family, while both tandem and segmental duplications contributed to the expansion of the potato MATE family, indicating that MATEs took distinct evolutionary paths in these two Solanaceous species. Analysis of ω values showed that all potato and pepper MATE genes experienced purifying selection during evolution. In addition, collinearity analysis showed that MATE genes were highly conserved between pepper and potato. Analysis of cis-elements in MATE promoters and MATE expression patterns revealed that MATE proteins likely function in many stages of plant development, especially during fruit ripening, and when exposed to multiple stresses, consistent with the existence of functional differentiation between duplicated MATE genes. Together, our results lay the foundation for further characterization of pepper and potato MATE gene family members.

Membrane Attack Complex and Perforin (MACPF) proteins play crucial roles in plant development and plant responses to environmental stresses. To date, only four MACPF genes have been identified in Arabidopsis thaliana, and the functions of the MACPF gene family members in other plants, especially in important crop plants, such as the Poaceae family, remain largely unknown. In this study, we identified and analyzed 42 MACPF genes from six completely sequenced and well annotated species representing the major Poaceae clades. A phylogenetic analysis of MACPF genes resolved four groups, characterized by shared motif organizations and gene structures within each group. MACPF genes were unevenly distributed along the Poaceae chromosomes. Moreover, segmental duplications and dispersed duplication events may have played significant roles during MACPF gene family expansion and functional diversification in the Poaceae. In addition, phylogenomic synteny analysis revealed a high degree of conservation among the Poaceae MACPF genes. In particular, Group I, II, and III MACPF genes were exposed to strong purifying selection with different evolutionary rates. Temporal and spatial expression analyses suggested that Group III MACPF genes were highly expressed relative to the other groups. In addition, most MACPF genes were highly expressed in vegetative tissues and up-regulated by several biotic and abiotic stresses. Taken together, these findings provide valuable information for further functional characterization and phenotypic validation of the Poaceae MACPF gene family.

Immune response in plants is tightly regulated by the coordination of the cell surface and intracellular receptors. In animals, the membrane attack complex/perforin-like (MACPF) protein superfamily creates oligomeric pore structures on the cell surface during pathogen infection. However, the function and molecular mechanism of MACPF proteins in plant pathogen responses remain largely unclear. In this study, we identified an Arabidopsis MACP2 and investigated the responsiveness of this protein during both bacterial and fungal pathogens. We suggest that MACP2 induces programmed cell death, bacterial pathogen resistance, and necrotrophic fungal pathogen sensitivity by activating the biosynthesis of tryptophan-derived indole glucosinolates and the salicylic acid signaling pathway dependent on the activity of enhanced disease susceptibility 1 (EDS1). Moreover, the response of MACP2 mRNA isoforms upon pathogen attack is differentially regulated by a posttranscriptional mechanism: alternative splicing. In comparison to previously reported MACPFs in Arabidopsis, MACP2 shares a redundant but nonoverlapping role in plant immunity. Thus, our findings provide novel insights and genetic tools for the MACPF family in maintaining SA accumulation in response to pathogens in Arabidopsis.

The Membrane Attack Complex and Perforin (MACPF) proteins play a crucial role in plant development and adaptation to environmental stresses. Heretofore, few MACPF genes have been functionally identified, leaving gaps in our understanding of MACPF genes in other plants, particularly in the Solanaceae family, which includes economically and culturally significant species, such as tomato, potato, and pepper. In this study, we have identified 26 MACPF genes in three Solanaceae species and in the water lily, which serves as the base group for angiosperms. Phylogenetic analysis indicates that angiosperm MACPF genes could be categorized into three distinct groups, with another moss and spikemoss lineage-specific group, which is further supported by the examination of gene structures and domain or motif organizations. Through inter-genome collinearity analysis, it is determined that there are 12 orthologous SolMACPF gene pairs. The expansion of SolMACPF genes is primarily attributed to dispersed duplications, with purifying selection identified as the principal driving force in their evolutionary process, as indicated by the ω values. Furthermore, the analysis of expression patterns revealed that Solanaceae genes are preferentially expressed in reproductive tissues and regulated by various environmental stimuli, particularly induced by submergence. Taken together, these findings offer valuable insights into and a fresh perspective on the evolution and function of SolMACPF genes, thereby establishing a foundation for further investigations into their phenotypic and functional characteristics.