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

Abstract

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.

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

“…The importance of multiple hormones in shade-regulated morphogenesis prompted us to focus on GO terms associated with hormone responses (Tao et al, 2008;Hornitschek et al, 2012;Li et al, 2012;Bou-Torrent et al, 2014;Procko et al, 2014;Nozue et al, 2015). Consistent with the early role of auxin in this process, the term response to auxin was significantly overrepresented among genes upregulated by shade both in hypocotyls and cotyledons at all time points of our analysis ( Figure 2C).…”

“…In response to additional FR light mimicking neighbor detection (low R/FR, referred to as shade), we observed enhanced hypocotyl elongation in Arabidopsis seedlings after approximately 1 h of shade treatment ( Figure 1A; Supplemental Figure 1A). Given that shade-induced hypocotyl growth is likely due to an increase in auxin (indole-3-acetic acid [IAA]) concentration (Tao et al, 2008;Keuskamp et al, 2010;Hornitschek et al, 2012;Li et al, 2012;Procko et al, 2014), we indirectly determined auxin levels in the hypocotyl using the DII-VENUS auxin sensor (Brunoud et al, 2012). We observed a reduction of the DII-VENUS signal in the hypocotyl within 1 h, indicating increased auxin levels ( Figure 1B).…”

“…The reduction in blue light typical of true shade is sensed by the cryptochrome photoreceptors (Sellaro et al, 2010;Keller et al, 2011;Pedmale et al, 2016). In young seedlings, cotyledons are considered to be the primary site of low R/FR perception; nevertheless, several studies have shown that other parts of the plant can also sense this light cue (Morgan et al, 1980;Tanaka et al, 2002;Procko et al, 2014;Nito et al, 2015).…”

“…Low R/FR releases phyB-mediated inhibition of several PIFs, leading to shade-induced elongation of hypocotyls and petioles (Lorrain et al, 2008;Keller et al, 2011;Leivar et al, 2012;Li et al, 2012;de Wit et al, 2015;Mizuno et al, 2015;Nozue et al, 2015). Shade-induced auxin biosynthesis in the cotyledons and young leaves followed by transport of the phytohormone into the hypocotyl is considered essential to trigger hypocotyl elongation (Steindler et al, 1999;Tao et al, 2008;Keuskamp et al, 2010;de Wit et al, 2014;Procko et al, 2014Procko et al, , 2016. In response to shade, PIF transcription factors directly regulate the expression of auxin biosynthesis and auxin response genes, thereby providing a link between environmental perception and the growth response (Hornitschek et al, 2012;Li et al, 2012;Hersch et al, 2014;Nozue et al, 2015).…”

“…We concentrated our analysis on these two organs because the former is considered to be the primary shade-sensing organ, while elongation is rapidly triggered in the hypocotyl (Tao et al, 2008;Cole et al, 2011;de Wit et al, 2014;Procko et al, 2014). Genetic experiments were designed based on interesting expression patterns, enabling us to test current models of shade-regulated hypocotyl elongation.…”