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Authors: Enrico Scarpella
Plant Physiology (2023)
Abstract: "For multicellular organisms to develop, cells must grow, divide, and differentiate along preferential or exclusive orientations or directions. Moreover, those orientations—or axes—and directions—or polarities—must be coordinated between cells within and between tissues. Therefore, how axes and polarities are coordinated between cells is a key question in biology. In animals, such coordination mainly depends on cell migration and direct interaction between proteins protruding from the plasma membrane. Both cell movements and direct cell–cell interactions are prevented in plants by cell walls that surround plant cells and keep them apart and in place. Therefore, plants have evolved unique mechanisms to coordinate their cell axes and polarities. Here I will discuss evidence suggesting that understanding how leaf veins form may uncover those unique mechanisms. Indeed—unlike previously thought—the cell-to-cell, polar transport of the plant hormone auxin along developing veins cannot account for many features of vein patterning. Instead, those features can be accounted for by models of vein patterning that combine polar auxin transport with auxin diffusion through plasmodesmata along the axis of developing veins. Though it remains unclear whether such a combination of polar transport and axial diffusion of auxin can account for the formation of the variety of vein patterns found in plant leaves, evidence suggests that such a combined mechanism may control plant developmental processes beyond vein patterning."
Authors: Jesse J. Küpers, Basten L. Snoek, Lisa Oskam, Chrysoula K. Pantazopoulou, Sanne E. A. Matton, Emilie Reinen, Che-Yang Liao, Eline D. C. Eggermont, Harold Weekamp, Muthanna Biddanda-Devaiah, Wouter Kohlen, Dolf Weijers and Ronald Pierik.
Current Biology (2023)
Highlights: • Temporal transcriptome patterns in response to shade cues in leaf segments • Tissue-specific quantification of auxin reporter in petioles • Auxin and Gibberellin interactively regulate leaf movement • Mechanisms underpinning physical separation of light signaling and response
Abstract: "Although plants are immobile, many of their organs are flexible to move in response to environmental cues. In dense vegetation, plants detect neighbors through far-red light perception with their leaf tip. They respond remotely, with asymmetrical growth between the abaxial and adaxial sides of the leafstalk, the petiole. This results in upward movement that brings the leaf blades into better lit zones of the canopy. The plant hormone auxin is required for this response, but it is not understood how non-differential leaf tip-derived auxin can remotely regulate movement. Here, we show that remote signaling of far-red light promotes auxin accumulation in the abaxial petiole. This local auxin accumulation is facilitated by reinforcing an intrinsic directionality of the auxin transport protein PIN3 on the petiole endodermis, as visualized with a PIN3-GFP line. Using an auxin biosensor, we show that auxin accumulates in all cell layers from endodermis to epidermis in the abaxial petiole, upon far-red light signaling in the remote leaf tip. In the petiole, auxin elicits a response to both auxin itself as well as a second growth promoter; gibberellin. We show that this dual regulation is necessary for hyponastic leaf movement in response to light. Our data indicate that gibberellin is required to permit cell growth, whereas differential auxin accumulation determines which cells can grow. Our results reveal how plants can spatially relay information about neighbor proximity from their sensory leaf tips to the petiole base, thus driving adaptive growth."
Authors: Batist Geldhof, Jolien Pattyn, Petar Mohorović, Karlien Van den Broeck, Vicky Everaerts, Ondřej Novák and Bram Van de Poel.
bioRxiv (2022)
Abstract: "Developing leaves undergo a vast array of age-related changes as they mature. These include physiological, hormonal and morphological changes that determine their adaptation plasticity towards adverse conditions. Waterlogging induces leaf epinasty in tomato, and the magnitude of leaf bending is intricately related to the age-dependent cellular and hormonal response. We now show that ethylene, the master regulator of epinasty, is differentially regulated throughout leaf development, giving rise to age-dependent epinastic responses. Young leaves have a higher basal ethylene production, but are less responsive to waterlogging-induced epinasty, as they have a higher capacity to convert the root-borne and mobilized ACC into the inactive conjugate MACC. Ethylene stimulates cell elongation relatively more at the adaxial petiole side, by activating auxin biosynthesis and locally inhibiting its transport through PIN4 and PIN9 in older and mature leaves. As a result, auxins accumulate in the petiole base of these leaves and enforce partially irreversible epinastic bending upon waterlogging. Young leaves maintain their potential to transport auxins, both locally and through the vascular tissue, leading to enhanced flexibility to dampen the epinastic response and a faster upwards repositioning during reoxygenation. This mechanism also explains the observed reduction of epinasty during and its recovery after waterlogging in the anthocyanin reduced (are) and Never ripe (Nr) mutants, both characterized by higher auxin flow. Our work has demonstrated that waterlogging activates intricate hormonal crosstalk between ethylene and auxin, controlled in an age-dependent way."
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Authors: Yanjun Zhang, Shaqila Han, Yuqing Lin, Jiyue Qiao, Naren Han, Yanyan Li, Yaning Feng, Dongming Li and Yanhua Qi.
Plants (2023)
Abstract: "Leaf inclination is one of the most important components of the ideal architecture, which effects yield gain. Leaf inclination was shown that is mainly regulated by brassinosteroid (BR) and auxin signaling. Here, we reveal a novel regulator of leaf inclination, auxin transporter OsPIN1b. Two CRISPR-Cas9 homozygous mutants, ospin1b-1 and ospin1b-2, with smaller leaf inclination compared to the wild-type, Nipponbare (WT/NIP), while overexpression lines, OE-OsPIN1b-1 and OE-OsPIN1b-2 have opposite phenotype. Further cell biological observation showed that in the adaxial region, OE-OsPIN1b-1 has significant bulge compared to WT/NIP and ospin1b-1, indicating that the increase in the adaxial cell division results in the enlarging of the leaf inclination in OE-OsPIN1b-1. The OsPIN1b was localized on the plasma membrane, and the free IAA contents in the lamina joint of ospin1b mutants were significantly increased while they were decreased in OE-OsPIN1b lines, suggesting that OsPIN1b might action an auxin transporter such as AtPIN1 to alter IAA content and leaf inclination. Furthermore, the OsPIN1b expression was induced by exogenous epibrassinolide (24-eBL) and IAA, and ospin1b mutants are insensitive to BR or IAA treatment, indicating that the effecting leaf inclination is regulated by OsPIN1b. This study contributes a new gene resource for molecular design breeding of rice architecture."
Authors: Qingqing Wang, Marco Marconi, Chunmei Guan, Krzysztof Wabnik and Yuling Jiao.
PNAS (2022)
Significance: "Flattened leaf blade formation is a key adaption of plants to the environment, but its developmental regulation remains to be resolved. Classical microsurgery experiments suggest that a mobile signal, known as the Sussex signal, in the shoot apex is required for flattened leaf formation. A recent study found that polar auxin transport contributes to the Sussex signal, but how microsurgeries interact with polarity genes remains elusive. Here, we combine live-imaging and computer model simulations to show that an oval-shaped auxin response in inner cells of leaf primordium is essential for the formation of bipolar SlLAM1 expression domain, which establishes initial bilateral leaf primordia. Microsurgeries lead to an axisymmetric domain shape and can interfere with other polarity factors.
Abstract: "The flattened leaf form is an important adaptation for efficient photosynthesis, and the developmental process of flattened leaves has been intensively studied. Classic microsurgery studies in potato and tomato suggest that the shoot apical meristem (SAM) communicates with the leaf primordia to promote leaf blade formation. More recently, it was found that polar auxin transport (PAT) could mediate this communication. However, it is unclear how the expression of leaf patterning genes is tailored by PAT routes originating from SAM. By combining experimental observations and computer model simulations, we show that microsurgical incisions and local inhibition of PAT in tomato interfere with auxin transport toward the leaf margins, reducing auxin response levels and altering the leaf blade shape. Importantly, oval auxin responses result in the bipolar expression of SlLAM1 that determines leaf blade formation. Furthermore, wounding caused by incisions promotes degradation of SlREV, a known regulator of leaf polarity. Additionally, computer simulations suggest that local auxin biosynthesis in early leaf primordia could remove necessity for external auxin supply originating from SAM, potentially explaining differences between species. Together, our findings establish how PAT near emerging leaf primordia determines spatial auxin patterning and refines SlLAM1 expression in the leaf margins to guide leaf flattening."
Authors: Ziyuan Peng, Daniel Alique, Yuanyuan Xiong, Jinrong Hu, Xiuwei Cao, Shouqin Lü, Mian Long, Ying Wang, Krzysztof Wabnik and Yuling Jiao.
Current Biology (2022)
Editor's view: Peng et al. show that different growth dynamics determine the shape of plant aerial organs, leaf and floral primordia, which share similar initial geometry. Experiments and simulations are combined to link growth dynamics with biomechanics and polar auxin transport.
Highlights: • Leaf and floral primordia share similar gene expression and initial domain partition • Local growth-rate differences across domains explain primordia shape differences • Two primordia have different patterns of cell-wall rigidity and auxin convergence • When incorporating growth dynamics, models explain different organ shapes
Abstract: "How gene activities and biomechanics together direct organ shapes is poorly understood. Plant leaf and floral organs develop from highly similar initial structures and share similar gene expression patterns, yet they gain drastically different shapes later—flat and bilateral leaf primordia and radially symmetric floral primordia, respectively. We analyzed cellular growth patterns and gene expression in young leaves and flowers of Arabidopsis thaliana and found significant differences in cell growth rates, which correlate with convergence sites of phytohormone auxin that require polar auxin transport. In leaf primordia, the PRESSED-FLOWER-expressing middle domain grows faster than adjacent adaxial domain and coincides with auxin convergence. In contrast, in floral primordia, the LEAFY-expressing domain shows accelerated growth rates and pronounced auxin convergence. This distinct cell growth dynamics between leaf and flower requires changes in levels of cell-wall pectin de-methyl-esterification and mechanical properties of the cell wall. Data-driven computer model simulations at organ and cellular levels demonstrate that growth differences are central to obtaining distinct organ shape, corroborating in planta observations. Together, our study provides a mechanistic basis for the establishment of early aerial organ symmetries through local modulation of differential growth patterns with auxin and biomechanics."
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