Modulation of root growth by nutrient-defined fine-tuning of polar auxin transport

Abstract

27Nitrogen is an essential macronutrient and its availability in soil plays a critical role in plant 28 growth, development and impacts agricultural productivity. Plants have evolved different 29 strategies to sense and respond to heterogeneous nitrogen distribution. Modulating root system 30 architecture, including primary root growth and branching, is among the most essential plant 31 adaptions to ensure adequate nitrogen acquisition. However, the immediate molecular 32 pathways coordinating the adjustment of root growth in response to varying nitrogen sources 33 are poorly understood. Here, using a combination of physiological, live in vivo high-and super 34 resolution imaging, we describe a novel adaptation strategy of root growth on available 35 nitrogen source. We show that growth, i.e. tissue-specific cell division and elongation rates are 36 fine-tuned by modulating auxin flux within and between tissues. Changes in auxin 37 redistribution are achieved by nitrogen source dependent post-translational modification of 38 PIN2, a major auxin efflux carrier, at an uncharacterized, evolutionary conserved phosphosite. 39 Further, we generate a computer model based on our results which successfully recapitulate 40 our experimental observations and creates new predictions that could broaden our 41 understanding of root growth mechanisms in the dynamic environment.42 43 48 determinants of plant growth and development. Although required, fluctuations in their 49 availabilities either to sub-or supra-optimal levels often have detrimental effects on plant 50 metabolism and physiology, thereby attenuating plant fitness. Hence, the acquisition of mineral 51 nutrients from the soil needs to be tightly controlled and endogenous levels within a plant body 52 maintained at a physiological optimum level. At the molecular level, balancing nutrient 53 acquisition with the plant's requirements implies that there is close communication between 54 pathways controlling uptake, distribution and homeostasis of nutrients and the pathways 55 coordinating plant growth and development.56 The root system perceives and integrates local and systemic signals on the nutrient 57 status to regulate activity of pathways mediating nutrient uptake and distribution. An important 58 3 component of the plant's nutrient management strategy involves a rapid modulation of the root 59 growth and development. In response to nutrient availability, root meristem activity and 60 elongation growth of primary root, as well as root branching, are adjusted in order to optimize 61 nutrient provision to the plant body 1 . Production of new cells is essential for sustainable root 62 growth; however, enhancement of the cell division machinery typically occurs within a range 63 of hours 2 . In contrast, rapid modulation of cell elongation and manifold increase in cell volume 64 would ensure faster growth responses 3 . Hence, in fluctuating environmental conditions root 65 growth kinetics relies on the coordination of rapid elongation growth and adjustment of 66 pr...

Dissecting Hierarchies between Light, Sugar and Auxin Action Underpinning Root and Root Hair Growth

“…Previously published studies linked the root illumination status and sucrose supplementation of the growth medium to altered root trait establishment, including differences in total root length and root hair outgrowth [ 1 , 25 , 41 ]. The establishment of those root traits depends strongly on fine-tuned polar auxin distribution, mediated by the auxin efflux carrier PIN2, through the root tip and availability of resources delivering energy to maintain proper root growth, in correlation to exogenous stimuli, like changing illumination or nutrition levels [ 3 , 11 , 23 , 25 , 26 ]. With this study, we present a first attempt to dissect the interplay between shootward transported auxin by PIN2, illumination status of the root and sucrose supplementation to the growth medium to mediate root growth and root hair outgrowth.…”

“…The root of Arabidopsis thaliana is an established model system to study molecular processes underpinning plant growth adaptation upon changing environmental conditions [ 1 , 10 , 18 , 19 , 20 , 21 , 22 ]. All root growth aspects are highly dependent on fine-tuned, active polar auxin distribution through the root tip followed by auxin signaling orchestrating cellular responses [ 3 , 11 , 23 , 24 , 25 , 26 ]. The auxin efflux transporter PIN-FORMED2 (PIN2) orchestrates root growth but is itself regulated on transcriptional through to the post-translational level by external factors such as nutrient availability or light [ 26 , 27 , 28 , 29 , 30 ].…”

“…All root growth aspects are highly dependent on fine-tuned, active polar auxin distribution through the root tip followed by auxin signaling orchestrating cellular responses [ 3 , 11 , 23 , 24 , 25 , 26 ]. The auxin efflux transporter PIN-FORMED2 (PIN2) orchestrates root growth but is itself regulated on transcriptional through to the post-translational level by external factors such as nutrient availability or light [ 26 , 27 , 28 , 29 , 30 ]. PIN2 abundance and subcellular distribution are dependent on light growth conditions for both the root and the shoot [ 25 , 29 , 30 ].…”

Interplay between Hormones and Several Abiotic Stress Conditions on Arabidopsis thaliana Primary Root Development

“…N is one of the most essential elements that restrict plant productivity and plants have developed strategies to avoid N limitation and to optimize its use during their life cycle [204]. Nitrate (NO 3 − ) is the major form of inorganic nitrogen source for Arabidopsis and, in many cases, at 5mM concentration, is able to induce PR growth by increasing meristem cell number and the length of completely elongated cells [205,206]. This effect probably depends on the ecotype used or on the methodological procedures [207,208].…”

The TOR–Auxin Connection Upstream of Root Hair Growth

“…Distribution of the phytohormone auxin through the plant creates auxin gradients, which orchestrate the activity of meristems, adaptational growth via cell expansion, and differentiation of specialized cells [ 12 , 13 , 14 , 15 ]. PIN-FORMED (PIN) proteins, auxin efflux carriers, ensure on-point and polar distribution of the phytohormone, whereby auxin signaling underpins the fine-tuning of various cellular processes involved in plant growth adaptation under changing environmental conditions [ 3 , 16 , 17 , 18 ]. The role of the root-specific PIN family member PIN2 during root hair growth adaptation in response to environmental conditions will be discussed in particular in the scope of this review.…”