Understanding the Intricate Web of Phytohormone Signalling in Modulating Root System Architecture

Abstract

Root system architecture (RSA) is an important developmental and agronomic trait that is regulated by various physical factors such as nutrients, water, microbes, gravity, and soil compaction as well as hormone-mediated pathways. Phytohormones act as internal mediators between soil and RSA to influence various events of root development, starting from organogenesis to the formation of higher order lateral roots (LRs) through diverse mechanisms. Apart from interaction with the external cues, root development also relies on the complex web of interaction among phytohormones to exhibit synergistic or antagonistic effects to improve crop performance. However, there are considerable gaps in understanding the interaction of these hormonal networks during various aspects of root development. In this review, we elucidate the role of different hormones to modulate a common phenotypic output, such as RSA in Arabidopsis and crop plants, and discuss future perspectives to channel vast information on root development to modulate RSA components.

Keywords: phytohormone signalling; root development; root meristem; root system architecture; root system plasticity; root tropic responses.

Figure 1

(A) Tap root system: RSA of a dicot (tomato) showing embryonic primary root, lateral roots, adventitious roots of shoot origin (hypocotyl root), and root-shoot junction (junction root). (B) Fibrous root system: RSA of a monocot (maize) showing embryonic origin primary root and seminal roots, adventitious roots of shoot origin (brace roots) and root-shoot junction (crown root), laterals, and root tip. (C) Root tip of primary root showing root cap, meristematic zone, elongation zone, and maturation zone having root hairs.

Figure 2

Regulation of primary root (PR) growth by various hormones and their crosstalk. (A) Auxin effects root growth in a concentration-dependent manner and interacts with ET signalling pathway to control PR elongation. Low concentration of auxin promotes PR growth probably via free AUX/IAAs, while high concentration inhibited PR growth through TIR1-mediated signalling via an unknown non-transcriptional mechanism (B) CK signalling modulates PR growth via AUX-1 mediated auxin translocation. (C) BR induces ET production via stabilizing ACS5, and ACS9 represses ET synthesis through BES1 and BZR1-mediated repression of ACS7, ACS9, and ACS11 to control PR growth. (D) MYC2, a DNA binding bHLH transcription factor in JA signalling, represses the transcriptional expression of PLT1 and PLT2. JA regulates expression of ASA1 and modulates auxin levels to cause root growth inhibition. JA and auxinsignalling occurs via AXR1 to control PR growth. (E) SA via NPR1-mediated signalling establishes an auto regulatory feedback regulation between CK2 and SA to link between SA signalling and auxin transport. SA also led to inhibition of PR elongation in NPR1-independent manner via affecting PP2A, leading to changes in PIN activity and auxin export, resulting in attenuation of root growth. Solid black arrow indicates confirmed pathway. Blue arrow indicates low levels of auxin, green arrow indicates high levels of auxin. Red circle indicates phosphorylation.

Figure 3

Regulation of LR development by various hormones and their crosstalk. Auxin via SLR4/ARF7-ARF9 signalling module promotes LR development. Auxin-induced expression of PRH1 is dependent on ARF7 and LBD29. PRH1 may promote LR development by regulating the expression of EXP genes that promote cell wall loosening. SLR4/ARF7-ARF9 signalling module also activates the expression of LBD16/ASL18 that are involved in the symmetry breaking of LR founder cells for LR initiation and primordium development. JA positively regulates lateral root formation by modulating auxin biosynthesis and homeostasis. JA induces the expression of ASA1 both through COI1 and ERF109. ERF109 also induces the expression of another auxin biosynthetic gene, YUC9. BR regulates lateral root development by interacting with auxin. At low concentration, BR modulates auxin transport and promotes lateral root development. CK negatively regulates LR initiation and development by inhibiting auxin carriers. Solid black arrows indicate confirmed pathway. Dotted arrow indicates pathways for which there is little or no evidence.

Figure 4

Regulation of AR development by various hormones and their crosstalk. Auxin controls AR initiation by activating ARF6 and ARF8, leading to downregulation of COI1-mediated JA signalling. GH3.3, GH3.5, and GH3.6 are regulated by ARF6, ARF8, and ARF17. The 3 GH3s control JA homeostasis. JA level controls JA-Ile levels. JA-Ile negatively regulates AR development by activating COI1-dependent signalling. Feedback regulation by DAO1 is activated by JA signalling, which then regulates IAA homeostasis. SA at low concentration promotes AR development, whereas at higher concentrations it inhibits AR development. CK regulates auxin homeostasis by negatively affecting auxin carriers PIN, LAX, and YUCCA1 genes, thereby regulating adventitious rooting through these pathways. In poplar cuttings, CK signalling activates PtARR13, which represses AR formation by promoting the expression of PDR9 and inhibiting the expression of TINY-Like TF. Solid black arrows indicate confirmed pathway. Dotted arrow indicates pathways for which there is little or no evidence. Blue arrow indicates low level of SA and green arrow indicates high level of SA.

Figure 5

Regulation of RH development by various hormones and their crosstalk.BR positively regulates the expression of WER, GL2 (negative regulator of RH development) and inhibits BIN2, which is then unable to phosphorylate GL3/EGL3 and TTG1. Presence of BR promotes functional TF complex formation between TTG1, GL3/EGL3, and WER, promoting GL2 expression, leading to inhibition of the RH development pathway. CK induces TF ZFP5, which promotes the expression of CPC (positive regulator of RH development), leading to the formation of functional TF complex of TTG1, GL3/EGL3, and CPC. The complex inhibits the expression of GL2, thus causing activation of the RH development pathway. The presence of auxin liberates the ARFs from AUX/IAAs. The ARFs show different specificity to RH development. ARF4-11 inhibits, whereas ARF6 promotes, the RH development pathway. ARF5 directly interacts with the promotor of RSL4, leading to RH development. Auxin also directly regulates the expression of RSL4 target gene ERU via ARF7/ARF19. JA positively influences RH growth via ET signalling. Solid black arrows indicate confirmed pathways.

Figure 6

Regulation of PR and LR gravitropism by various hormones and their crosstalk. (A) PABA works upstream of ET signalling, through which it regulates auxin biosynthesis and transport. This ultimately leads to ARF7/19 mediated auxin activity effects on asymmetric growth promotion followed by root gravitropic response. Glc acts via BR to regulate root gravitropism. BR regulates root gravitropism by interacting with auxin via PIN2 distribution. Auxin signalling module TIR1-AFB-IAA17 mediates starch granule formation and gravitropic perception by inhibiting the expression of PGM, ADG1, and SS4. JA influences gravitropic response by modulating auxin levels through SA1 induction. SA affects auxin transport and redistribution, leading to gravitropic bending. (B) The presence of JA activates COI1-mediated JA signalling that causes proteasomal degradation of JAZ9, leading to the liberation of MYC2, which then binds to the promotors of CYP79B2 and LAZ2 and LAZY4, leading to changes in auxin homeostasis and LR gravitropism. Auxin transport and signalling modules are essential to regulate vertical orientation of LRs. The binding of FLP and MYB88 TFs leads to transcriptional activation of PIN3 and PIN7, which then lead to gravitropic bending of LRs. CK perturbs auxin homeostasis, leading to horizontal branching of LRs. Solid black arrows indicate confirmed pathways.