Claus Schwechheimer

Summary: In flowering plants, the timing of pollen germination is crucial for successful fertilization and an important trait for seed and fruit crops. Environmental factors tightly regulate pollen germination, with germination‐suppressing conditions on the pollen‐producing anther and germination‐promoting conditions on the receiving stigma. Using genetic, biochemical, and cell biological methods, we show that this environmental sensitivity of pollen germination in Arabidopsis thaliana is regulated by a 3‐PHOSPHOINOSITIDE‐DEPENDENT KINASE 1 (PDK1)‐AGC1.5/AGC1.7 kinase cascade. We show that PDK1 hyperphosphorylates downstream AGC1.5/7 kinases to enhance their activity. Pollen‐specific phosphoproteomics identified multiple proteins involved in pollen growth whose phosphorylation is controlled by AGC1.5/7. Two germination‐promoting RHO OF PLANTS GUANINE NUCLEOTIDE EXCHANGE FACTORS (ROPGEFs) are phosphorylated by AGC1.5/7 at a novel site, reducing ROPGEF plasma membrane polarization. Loss of PDK1‐AGC kinase signaling resulted in precocious pollen germination on the anther, which was rescued by high AGC1.5 kinase activity. Conversely, AGC1.5/7 overexpression or a phosphomimic ROPGEF version inhibited precocious pollen germination. Distinct subcellular localization of PDK1 and AGC1 kinases upon pollen germination is likely to alleviate their inhibitory effect. Our data indicate that the correct timing of pollen germination requires the fine‐tuned activity of a PDK1‐AGC1 kinase cascade inhibiting ROPGEFs on the anther, preventing precocious pollen germination.

In plants, the vascular network enables the transport of water, nutrients and metabolites. The vascular network formed in leaves is a striking example of tissue patterning, and leaf venation is a defining leaf feature. During patterning, veins arise from aligned, elongated procambial cells derived from undifferentiated ground meristem cells. The mechanisms behind procambial strand formation involving cell selection, polarization, alignment, elongation and division have remained elusive. Here we identify a previously uncharacterized role for the polar protein PAX in establishing coordinated cell and tissue polarity during this process. We uncover a novel, auxin-guided role for the polar PAX protein in establishing cell and tissue polarity that precedes and is independent of the polarization and activity of PIN auxin transporters. Our findings refine and redefine existing models of vascular patterning during vein network formation in plant leaves.

Summary: Plants continuously monitor their environment to adapt to threats affecting health and fitness. Cell‐surface receptors detect conserved microbe‐associated molecular patterns (MAMPs) or endogenous immunogenic signals to activate signaling pathways that induce broad‐spectrum disease resistance, known as pattern‐triggered immunity (PTI). In Arabidopsis thaliana , the leucine‐rich repeat receptor kinase MIK2 emerged as a versatile receptor involved in perceiving endogenous SCOOP peptides as well as potential MAMPs derived from Fusarium and related fungi. While SCOOP perception appears restricted to Brassicales, the Fusarium ‐derived elicitor triggers PTI responses across different plant lineages. Here, we demonstrate that Fusarium elicitor responsiveness and MIK2‐clade proteins are conserved among seed plants. We identified a tomato MIK2‐clade receptor that shares At MIK2 properties in perceiving the Fusarium elicitor, but not SCOOPs. Tomato mutants lacking the receptor show compromised PTI responses to the fungal elicitor and increased susceptibility to Fusarium oxysporum . By integrating AI‐assisted structural prediction with experimental data, we identify conserved and variable residues in Arabidopsis and tomato MIK2‐clade receptors that may underlie shared and lineage‐specific recognition specificities. Together, these findings establish MIK2‐clade receptors as immune surveillance modules that have undergone lineage‐specific diversification, supporting a model in which endogenous danger perception might have evolved from an ancestral role in microbial pattern recognition.

In flowering plants, the correct timing of pollen germination is crucial for successful fertilization and, therefore, an important trait for seed and fruit crops. Environmental factors tightly regulate pollen germination, with germination-suppressing conditions in the pollen-producing anther and germination-promoting conditions on the receiving stigma. Here we show that the differential environmental sensitivity of pollen germination in Arabidopsis thaliana is regulated by an AGC kinase cascade involving 3-PHOSPHOINOSITIDE-DEPENDENT KINASE 1 (PDK1) as upstream regulator, the AGC1.5 and AGC1.7 kinases as intermediate transducers and pollen germination promoting GUANINE NUCLEOTIDE EXCHANGE FACTORS (GEFs) as their likely phosphorylation targets. Loss of AGC kinase signaling resulted in precocious pollen germination in the anther, whereas AGC1.5/7 kinase overexpression or expression of a phosphomimic ROPGEF version inhibited pollen germination. Our data reveals that pollen germination requires the fine-tuned activity of an PDK1-AGC1 kinase cascade, preventing humidity-dependent precocious pollen germination on the anther.

Summary: We hypothesized that B‐GATA family transcription factors have important roles in growth regulation in moss. We analyzed B‐GATA family transcription factor mutants from Physcomitrium patens and Arabidopsis thaliana to assess growth, gene expression, and cytokinin‐related processes under varying nitrogen conditions. We found that nitrogen‐dependent growth and transcriptional regulation are strongly impaired in mutants from Physcomitrium and Arabidopsis . We detected altered cytokinin homeostasis or signaling in the mutants, linking hormonal imbalance to growth and transcription defects. We demonstrated a conserved, critical role of B‐GATAs in plant nitrogen‐responsive growth. Results suggest that B‐GATAs influence nitrogen‐regulated transcription downstream from cytokinin, supporting an ancient, evolutionarily conserved mechanism connecting nutrient signaling to growth. We provided experimental evidence for the long‐speculated but as‐yet not demonstrated role of GATA transcription factors in nitrogen‐dependent growth in land plants.

Summary: Plants continuously monitor their environment to adapt to threats affecting health and fitness. Cell-surface receptors detect conserved microbe-associated molecular patterns (MAMPs) or endogenous immunogenic signals to activate signaling pathways that induce broad-spectrum disease resistance, known as pattern-triggered immunity (PTI). In Arabidopsis thaliana , the leucine-rich repeat receptor kinase MIK2 emerged as a versatile receptor involved in perceiving endogenous SCOOP peptides as well as potential MAMPs derived from Fusarium and related fungi. While SCOOP perception appears restricted to Brassicales, the Fusarium -derived elicitor triggers PTI-responses across different plant lineages. Here, we demonstrate that Fusarium elicitor-responsiveness and MIK2-clade proteins are conserved among seed plants. We identified a tomato MIK2-clade receptor that shares At MIK2 properties in perceiving the Fusarium elicitor, but not SCOOPs. Tomato mutants lacking the receptor show compromised PTI-responses to the fungal elicitor and increased susceptibility to Fusarium oxysporum . By integrating AI-assisted structural prediction with experimental data, we identify conserved and variable residues in Arabidopsis and tomato MIK2-clade receptors that may underlie shared and lineage-specific recognition specificities. Together, these findings establish MIK2-clade receptors as immune surveillance modules that have undergone lineage-specific diversification, supporting a model in which endogenous danger perception might have evolved from an ancestral role in microbial pattern recognition.

Plants use environmental cues to orient organ and plant growth, such as the direction of gravity or the direction, quantity, and quality of light. During the germination of Arabidopsis thaliana seeds in soil, negative gravitropism responses direct hypocotyl elongation such that the seedling can reach the light for photosynthesis and autotrophic growth. Similarly, hypocotyl elongation in the soil also requires mechanisms to efficiently grow around obstacles such as soil particles. Here, we identify KIPK (KINESIN-LIKE CALMODULIN-BINDING PROTEIN-INTERACTING PROTEIN KINASE) and the paralogous KIPKL1 (KIPK-LIKE1) as genetically redundant regulators of gravitropic hypocotyl bending. Moreover, we demonstrate that the homologous KIPKL2 (KIPK-LIKE2), which shows strong sequence similarity, must be functionally distinct. KIPK and KIPKL1 are polarly localized plasma membrane-associated proteins that can activate PIN-FORMED auxin transporters. KIPK and KIPKL1 are required to efficiently align hypocotyl growth with the gravity vector when seedling hypocotyls are grown on media plates or in soil, where contact with soil particles and obstacle avoidance impede direct negative gravitropic growth. Therefore, the polar KIPK and KIPKL1 kinases have different biological functions from the related AGC1 family kinases D6PK (D6 PROTEIN KINASE) or PAX (PROTEIN KINASE ASSOCIATED WITH BRX).

Plants use environmental cues, such as the direction of gravity or the direction, quantity and quality of light, to orientate organ and plant growth. During germination of angiosperm seeds in the soil, hypocotyl elongation is directed by negative gravitropism responses such that the seedling can reach the light for photosynthesis and autotrophic growth. Hypocotyl elongation in the soil, however, also requires mechanisms to efficiently grow around obstacles such as soil particles. Here, we identify KIPK (KINESIN-LIKE CALMODULIN-BINDING PROTEIN INTERACTING PROTEIN KINASE) and the paralogous KIPKL1 (KIPK-LIKE1) as genetically redundant regulators of hypocotyl bending, in that KIPK and KIPKL1 are required to efficiently align hypocotyl growth with the gravity vector after obstacle avoidance. At the same time, we find that the highly homologous KIPKL2 (KIPK-LIKE2) must be functionally distinct. We further find that KIPK, and likely also KIPKL1, phosphorylate BRXL2 (BREVIS RADIX LIKE2) and ARKs (ARMADILLO REPEAT KINESINs), that mutants of both KIPK phosphorylation substrates share the overbending phenotype with kipk kipkl1 mutants, and that KIPK and KIPKL1 act synergistically with the ARK-regulatory NEK6 ( NIMA-RELATED PROTEIN KINASE6 ). We propose that KIPK and KIPKL1 regulate ARK kinesins and thereby cortical microtubules for efficient gravitropic hypocotyl bending.

Plant pathogens pose a high risk of yield losses and threaten food security. Technological and scientific advances have improved our understanding of the molecular processes underlying host-pathogen interactions, which paves the way for new strategies in crop disease management beyond the limits of conventional breeding. Cross-family transfer of immune receptor genes is one such strategy that takes advantage of common plant immune signaling pathways to improve disease resistance in crops. Sensing of microbe- or host damage-associated molecular patterns (MAMPs/DAMPs) by plasma membrane-resident pattern recognition receptors (PRR) activates pattern-triggered immunity (PTI) and restricts the spread of a broad spectrum of pathogens in the host plant. In the model plant Arabidopsis thaliana , the S-domain receptor-like kinase LIPOOLIGOSACCHARIDE-SPECIFIC REDUCED ELICITATION ( At LORE, SD1-29) functions as PRR, which senses medium chain-length 3-hydroxylated fatty acids (mc-3-OH-FAs), such as 3-OH-C10:0, and 3-hydroxyalkanoates (HAAs) of microbial origin to activate PTI. In this study, we show that ectopic expression of the Brassicaceae-specific PRR At LORE in the solanaceous crop species Solanum lycopersicum cv. M82 leads to the gain of 3-OH-C10:0 immune sensing without altering plant development. AtLORE -transgenic tomato shows enhanced resistance against Pseudomonas syringae pv. tomato DC3000 and Alternaria solani NL03003. Applying 3-OH-C10:0 to the soil before infection induces resistance against the oomycete pathogen Phytophthora infestans Pi100 and further enhances resistance to A. solani NL03003. Our study proposes a potential application of AtLORE -transgenic crop plants and mc-3-OH-FAs as resistance-inducing bio-stimulants in disease management.