Stem Transcriptome Reveals Mechanisms to Reduce the Energetic Cost of Shade-Avoidance Responses in Tomato

Cagnola, Juan Ignacio; Ploschuk, Edmundo L.; Benech-Arnold, Tomás; Finlayson, Scott A.; Casal, Jorge J.

doi:10.1104/pp.112.201921

Cited by 92 publications

(104 citation statements)

References 47 publications

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“…The effects of ethylene on photosynthesis can be positive or negative depending on the context (Tholen et al, 2007;Iqbal et al, 2012). Low R:FR light-treated stems of tomato (Solanum lycopersicum) showed reduced expression of photosynthetic genes (Cagnola et al, 2012). This reduction was mainly due to a decrease in the expression of Calvin cycle genes, which we also observed for our Common Down set (Supplemental Table S1).…”

Section: Hypocotyl Growth Promotion and Photosynthesis Repression Occsupporting

confidence: 59%

Ethylene- and shade-induced hypocotyl elongation share transcriptome patterns and functional regulators

et al. 2016

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Plants have evolved shoot elongation mechanisms to escape from diverse environmental stresses such as flooding and vegetative shade. The apparent similarity in growth responses suggests a possible convergence of the signaling pathways. Shoot elongation is mediated by passive ethylene accumulating to high concentrations in flooded plant organs and by changes in light quality and quantity under vegetation shade. Here, we study hypocotyl elongation as a proxy for shoot elongation and delineate Arabidopsis (Arabidopsis thaliana) hypocotyl length kinetics in response to ethylene and shade. Based on these kinetics, we further investigated ethylene-and shade-induced genome-wide gene expression changes in hypocotyls and cotyledons separately. Both treatments induced a more extensive transcriptome reconfiguration in the hypocotyls compared with the cotyledons. Bioinformatics analyses suggested contrasting regulation of growth promotion-and photosynthesis-related genes. These analyses also suggested an induction of auxin, brassinosteroid, and gibberellin signatures and the involvement of several candidate regulators in the elongating hypocotyls. Pharmacological and mutant analyses confirmed the functional involvement of several of these candidate genes and physiological control points in regulating stress-escape responses to different environmental stimuli. We discuss how these signaling networks might be integrated and conclude that plants, when facing different stresses, utilize a conserved set of transcriptionally regulated genes to modulate and fine-tune growth.

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Section: Hypocotyl Growth Promotion and Photosynthesis Repression Occsupporting

confidence: 59%

Ethylene- and shade-induced hypocotyl elongation share transcriptome patterns and functional regulators

et al. 2016

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“…Such a response pattern is compatible with the opposite growth responses of these organs, given that ABA is rather growth inhibiting. Tomato (Solanum lycopersicum) plants subjected to long-term shade treatments and the constitutively shade-avoiding phyB mutant (in Arabidopsis) have higher ABA levels in leaves than in hypocotyls, but it is currently unknown whether shade leads to rapid changes in ABA levels and what the consequences of such changes are (Cagnola et al, 2012;González et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

“…Stems and hypocotyls elongate, petioles adopt a more upright position (hyponasty) and elongate, while leaf blade growth is often reduced and branching is inhibited (Kozuka et al, 2010;Casal, 2013;Reddy et al, 2013;de Wit et al, 2015). It is generally accepted that these organ-specific growth responses are the result of resource reallocation and are favorable to maximize growth and survival in an environment with limited light availability (Cagnola et al, 2012;Casal, 2013).…”

Section: Introductionmentioning

confidence: 99%

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

et al. 2016

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ORCID IDs: 0000-0001-5075-575X (M.V.K.); 0000-0003-1339-5120 (E.S.-S.); 0000-0002-4145-7205 (F.S.); 0000-0001-9237-1797 (P.M.-M.); 0000-0002-9623-2599 (J.M.); 0000-0002-3413-6841 (I.X.); 0000-0003-4719-5901 (C.F.)In response to neighbor proximity, plants increase the growth of specific organs (e.g., hypocotyls) to enhance access to sunlight. Shade enhances the activity of Phytochrome Interacting Factors (PIFs) by releasing these bHLH transcription factors from phytochrome B-mediated inhibition. PIFs promote elongation by inducing auxin production in cotyledons. In order to elucidate spatiotemporal aspects of the neighbor proximity response, we separately analyzed gene expression patterns in the major light-sensing organ (cotyledons) and in rapidly elongating hypocotyls of Arabidopsis thaliana. PIFs initiate transcriptional reprogramming in both organs within 15 min, comprising regulated expression of several early auxin response genes. This suggests that hypocotyl growth is elicited by both local and distal auxin signals. We show that cotyledon-derived auxin is both necessary and sufficient to initiate hypocotyl growth, but we also provide evidence for the functional importance of the local PIFinduced response. With time, the transcriptional response diverges increasingly between organs. We identify genes whose differential expression may underlie organ-specific elongation. Finally, we uncover a growth promotion gene expression signature shared between different developmentally regulated growth processes and responses to the environment in different organs.

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“…One possibility is that this response regulates other aspects of the shade avoidance phenotype; for example, the down-regulation of defense genes in the hypocotyl (Cerrudo et al, 2012) or the reduction of stem photosynthetic capacity (Cagnola et al, 2012). Alternatively, the cotyledon-independent response might potentiate the response of hypocotyl cells to cotyledon-derived growth signals.…”

Section: Shade-induced Hypocotyl Growth Is Correlated With Epidermal mentioning

confidence: 99%

Cotyledon-Generated Auxin Is Required for Shade-Induced Hypocotyl Growth in Brassica rapa

et al. 2014

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Plant architecture is optimized for the local light environment. In response to foliar shade or neighbor proximity (low red to far-red light), some plant species exhibit shade-avoiding phenotypes, including increased stem and hypocotyl growth, which increases the likelihood of outgrowing competitor plants. If shade persists, early flowering and the reallocation of growth resources to stem elongation ultimately affect the yield of harvestable tissues in crop species. Previous studies have shown that hypocotyl growth in low red to far-red shade is largely dependent on the photoreceptor phytochrome B and the phytohormone auxin. However, where shade is perceived in the plant and how auxin regulates growth spatially are less well understood. Using the oilseed and vegetable crop species Brassica rapa, we show that the perception of low red to far-red shade by the cotyledons triggers hypocotyl cell elongation and auxin target gene expression. Furthermore, we find that following shade perception, elevated auxin levels occur in a basipetal gradient away from the cotyledons and that this is coincident with a gradient of auxin target gene induction. These results show that cotyledon-generated auxin regulates hypocotyl elongation. In addition, we find in mature B. rapa plants that simulated shade does not affect seed oil composition but may affect seed yield. This suggests that in field settings where mutual shading between plants may occur, a balance between plant density and seed yield per plant needs to be achieved for maximum oil yield, while oil composition might remain constant.

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Stem Transcriptome Reveals Mechanisms to Reduce the Energetic Cost of Shade-Avoidance Responses in Tomato

Cited by 92 publications

References 47 publications

Ethylene- and shade-induced hypocotyl elongation share transcriptome patterns and functional regulators

Ethylene- and shade-induced hypocotyl elongation share transcriptome patterns and functional regulators

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

Cotyledon-Generated Auxin Is Required for Shade-Induced Hypocotyl Growth in Brassica rapa

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