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Trihelix transcription factors GTL1 and DF1 prevent aberrant root hair formation in an excess nutrient condition
New Phytologist ( IF 9.4 ) Pub Date : 2022-06-17 , DOI: 10.1111/nph.18255
Michitaro Shibata 1 , David S Favero 1 , Ryu Takebayashi 2 , Arika Takebayashi 1 , Ayako Kawamura 1 , Bart Rymen 1, 3 , Yoichiroh Hosokawa 2 , Keiko Sugimoto 1, 4
Affiliation  

Introduction

Plant biomass accumulation is generally limited by the availability of nutrients, particularly that of the three primary nutrients, nitrogen (N), phosphorus (P) and potassium (K). In addition to N, P and K; the elements carbon (C), hydrogen (H), oxygen (O), calcium (Ca), magnesium (Mg) and sulfur (S) are collectively called essential macronutrients. Boron (B), chlorine (Cl), iron (Fe), manganese (Mn), molybdenum (Mo), nickel (Ni) and zinc (Zn), however, are referred to as essential micronutrients. Generally, plants cannot survive or complete their life cycle without these essential nutrients. Furthermore, aluminum (Al), silicon (Si), sodium (Na) and cobalt (Co), the so-called beneficial elements, are known to improve growth and yield of some plant species. Fertilizer application is an effective means of increasing plant growth in conditions where nutrients are otherwise lacking (Barker & Pilbeam, 2015). However, excess fertilizer application can harm the environment in multiple ways, such as by reducing air, water and land quality as has been documented for P and N fertilizers used in parts of Europe, North America and Asia (Liu et al., 2010; Foley et al., 2011; MacDonald et al., 2011; Sutton et al., 2021). Although over-fertilization can reduce land quality, thus making it less conducive to plant growth, our knowledge regarding plant responses to excess nutrients pales in comparison to our understanding of responses associated with nutrient starvation.

Root hairs, which grow from the epidermis, impact nutrient uptake from the soil, as they increase the surface area of the root system. In Arabidopsis, root hairs generally initiate from trichoblasts, one of two types of epidermal cells specified during root development. Atrichoblasts, however, are root epidermal cells that do not produce hairs under normal conditions (Salazar-Henao et al., 2016). Root hair initiation, as well as growth of root hairs, is precisely regulated based on nutrient availability. For instance, inorganic phosphate (Pi) starvation promotes both root hair formation and growth. Under Pi starvation, root hair number is increased by the initiation of root hairs from atrichoblasts and also by the production of multiple hairs from a single epidermal cell (Ma et al., 2001). At the same time, root hair length increases nearly three-fold in low compared to high Pi conditions (Bates & Lynch, 1996). This response of increased root hair growth under low P availability in Arabidopsis is important for increasing P acquisition under P-limiting conditions (Bates & Lynch, 2000, 2001). Iron deficiency also strongly affects root hair development (Schmidt et al., 2000). In contrast to Pi starvation, however, Fe deficiency increases root hair branching rather than promoting ectopic root hair formation (Müller & Schmidt, 2004). These findings suggest that at least some environmental signals affect root hair development independently of each other (Schmidt & Schikora, 2001).

Several transcription factors (TFs) have been identified that play key roles regulating root hair development (Ishida et al., 2008; Bruex et al., 2012; Shibata & Sugimoto, 2019; Vissenberg et al., 2020). Atrichoblasts are characterized specifically by the expression of GLABRA2 (GL2), which encodes a TF that functions as a negative regulator of root hair formation and is often used as a marker for nonhair cells (Di Cristina et al., 1996; Masucci et al., 1996; Lin et al., 2015). Conversely, the basic helix-loop-helix (bHLH) TFs ROOT HAIR DEFECTIVE6 (RHD6) and RHD6-LIKE1 (RSL1) are key factors that promote hair development (Masucci & Schiefelbein, 1994; Menand et al., 2007; Pires et al., 2013). Following specification of root epidermal cells as trichoblasts, RHD6 and RSL1 promote transcription of genes encoding other bHLHs, including RSL2, RSL4 and Lotus japonicus ROOTHAIRLESS-LIKE 3 (LRL3) (Masucci & Schiefelbein, 1994; Karas et al., 2009; Yi et al., 2010). The rsl2 rsl4 double mutant completely lacks root hairs (Yi et al., 2010), indicating that RSL2 and/or RSL4 are essential for root hair growth. Similarly, the double or triple mutants for LRL3 and its homologs LRL1 and/or LRL2 have short root hairs that occur at a lower density than normal (Karas et al., 2009; Tam et al., 2015; Breuninger et al., 2016). Thus LRL3, together with LRL1 and LRL2, contributes to both root hair formation and growth. In addition to promoting growth of root hairs in response to developmental signals, bHLHs, particularly RSL2 and RSL4, are also important for root hair growth induced by exogenous phytohormone (auxin, cytokinin, ethylene or jasmonic acid) treatments or nutrient (Pi, N or Fe) deficiency (Yi et al., 2010; Datta et al., 2015; Zhang et al., 2016; Feng et al., 2017; Mangano et al., 2017; Bhosale et al., 2018; X. Han et al., 2020; Qiu et al., 2021). Therefore, RSL2 and RSL4 appear to be core factors in the gene regulatory network (GRN) that controls root hair growth (Lee & Cho, 2013; Franciosini et al., 2017; Shibata & Sugimoto, 2019). In addition to these positive regulators of root hair growth, negative regulators have also been identified. The trihelix TF GT2-LIKE1 (GTL1) and its closest homolog, DF1, terminate root hair growth by directly repressing RSL4 together with RSL4 target-genes (Shibata et al., 2018). In addition, a DOF-type TF, OBF BINDING PROTEIN 4 (OBP4), is a negative regulator of root hair growth, as induction of OBP4 reduces root hair length (Rymen et al., 2017). Unlike GTL1 and DF1, OBP4 represses RSL2 expression and does not affect RSL4 expression, suggesting that plants have at least two transcriptional pathways that repress root hair growth.

Here we investigated how Arabidopsis root hairs are affected by the presence of multiple nutrients in excess. Specifically, we demonstrate that root hair growth is strongly suppressed on double-strength Murashige–Skoog (2×MS) medium. Further, we show that the gtl1-1 df1-1 mutant forms frail root hairs on 2×MS, suggesting that GTL1 and DF1 prevent aberrant root hair development in the presence of excess nutrients. These findings shed light on the mechanisms that plants have evolved to adapt to growth in variable conditions.



中文翻译:

Trihelix 转录因子 GTL1 和 DF1 在营养过剩的情况下防止异常根毛形成

介绍

植物生物量的积累通常受到养分可用性的限制,特别是氮 (N)、磷 (P) 和钾 (K) 这三种主要养分的可用性。除了 N、P 和 K;元素碳 (C)、氢 (H)、氧 (O)、钙 (Ca)、镁 (Mg) 和硫 (S) 统称为必需常量营养素。然而,硼 (B)、氯 (Cl)、铁 (Fe)、锰 (Mn)、钼 (Mo)、镍 (Ni) 和锌 (Zn) 被称为必需微量营养素。一般来说,如果没有这些必需营养素,植物就无法生存或完成其生命周期。此外,众所周知,所谓的有益元素铝 (Al)、硅 (Si)、钠 (Na) 和钴 (Co) 可以改善某些植物物种的生长和产量。 2015 年)。然而,过量施肥会以多种方式损害环境,例如降低空气、水和土地质量,正如欧洲、北美和亚洲部分地区使用的 P 和 N 肥料所记录的那样(Liu等人,  2010 年; Foley等人,  2011 年;MacDonald等人,  2011 年;Sutton等人,  2021 年)。尽管过度施肥会降低土地质量,从而使其不利于植物生长,但与我们对与营养缺乏相关的反应的理解相比,我们对植物对过量养分的反应的了解相形见绌。

从表皮生长的根毛会影响土壤对养分的吸收,因为它们会增加根系的表面积。在拟南芥中,根毛通常从毛细胞开始,毛细胞是根发育过程中指定的两种表皮细胞之一。然而,成纤维细胞是在正常条件下不产生毛发的根表皮细胞(Salazar-Henao等人,  2016 年)。根毛的萌发以及根毛的生长是根据养分的有效性进行精确调节的。例如,无机磷酸盐 (Pi) 饥饿促进了根毛的形成和生长。在 Pi 饥饿的情况下,根毛数量通过从成纤维细胞开始产生根毛以及从单个表皮细胞产生多根毛而增加(Ma等人,  2001 年)。同时,与高 Pi 条件相比,低 Pi 条件下的根毛长度增加了近三倍(Bates & Lynch,  1996 年)。拟南芥中低磷利用率下根毛生长增加的反应对于在磷限制条件下增加磷获取很重要(Bates & Lynch,  2000 , 2001)。缺铁也会严重影响根毛的发育(Schmidt,  2000)。然而,与 Pi 饥饿相比,Fe 缺乏会增加根毛的分枝,而不是促进异位根毛的形成 (Müller & Schmidt,  2004)。这些发现表明,至少有一些环境信号会相互独立地影响根毛的发育(Schmidt & Schikora,  2001)。

已鉴定出几种转录因子 (TF),它们在调节根毛发育方面发挥关键作用(Ishida等人,  2008 年;Bruex等人,  2012 年;Shibata 和 Sugimoto,  2019 年;Vissenberg等人,  2020 年)。Atrichoblasts 的特点是GLABRA2 ( GL2 ) 的表达,其编码作为根毛形成负调节因子的 TF,通常用作非毛细胞的标记物 (Di Cristina et al .,  1996 ; Masucci et al .。 ,  1996 ; 林等人, 2015 年)。相反,基本的 helix-loop-helix (bHLH) TFs ROOT HAIR DEFECTIVE6 (RHD6) 和 RHD6-LIKE1 (RSL1) 是促进头发发育的关键因素 (Masucci & Schiefelbein,  1994 ; Menand等人,  2007 ; Pires等人.,  2013 年)。在将根表皮细胞指定为毛细胞后,RHD6 和 RSL1 促进编码其他 bHLH 的基因转录,包括RSL2RSL4Lotus japonicus ROOTHAIRLESS-LIKE 3 ( LRL3 ) (Masucci & Schiefelbein,  1994 ; Karas et al .,  2009 ; Yi et人, 2010 年)。rsl2 rsl4双突变体完全没有根毛 (Yi et al .,  2010 ),表明RSL2和/或RSL4对根毛生长至关重要。同样,LRL3 及其同源物 LRL1 和/或 LRL2 的双突变体或三突变体具有正常密度的短根毛(Karas等人,  2009;Tam等人,  2015;Breuninger等人,  2016)。因此,LRL3 与 LRL1 和 LRL2 一起有助于根毛的形成和生长。除了响应发育信号促进根毛的生长外,bHLHs,特别是 RSL2 和 RSL4,对于外源性植物激素(生长素、细胞分裂素、乙烯或茉莉酸)处理或营养物(Pi、N 或Fe) 缺乏(Yi et al .,  2010 ; Datta et al .,  2015 ; Zhang et al .,  2016 ; Feng et al .,  2017 ; Mangano et al .,  2017 ; Bhosale et al .,  2018 ; X. Han et al.人.,  2020 ; 邱等人,  2021)。因此,RSL2 和 RSL4 似乎是控制根毛生长的基因调控网络 (GRN) 中的核心因素(Lee & Cho,  2013 ; Franciosini et al .,  2017 ; Shibata & Sugimoto,  2019)。除了这些根毛生长的正调节剂外,还发现了负调节剂。trihelix TF GT2-LIKE1 (GTL1) 及其最接近的同源物 DF1 通过直接抑制RSL4和 RSL4 靶基因来终止根毛生长(Shibata等人,  2018)。此外,DOF 型 TF,OBF 结合蛋白 4 (OBP4),是根毛生长的负调节剂,因为OBP4的诱导会缩短根毛长度 (Rymen et al .,  2017 )。与 GTL1 和 DF1 不同,OBP4 抑制RSL2 的表达并且不影响RSL4的表达,这表明植物至少有两个抑制根毛生长的转录途径。

在这里,我们研究了拟南芥根毛如何受到多种营养素过量存在的影响。具体来说,我们证明在双强度 Murashige-Skoog (2×MS) 培养基上根毛生长受到强烈抑制。此外,我们显示gtl1-1 df1-1突变体在 2×MS 上形成脆弱的根毛,这表明 GTL1 和 DF1 在存在过量营养物的情况下防止异常根毛发育。这些发现揭示了植物进化以适应可变条件下生长的机制。

更新日期:2022-06-17
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