The role of strigolactones in root development

Abstract

Strigolactones (SLs) and their derivatives were recently defined as novel phytohormones that orchestrate shoot and root growth. Levels of SLs, which are produced mainly by plant roots, increase under low nitrogen and phosphate levels to regulate plant responses. Here, we summarize recent work on SL biology by describing their role in the regulation of root development and hormonal crosstalk during root deve-lopment. SLs promote the elongation of seminal/primary roots and adventitious roots (ARs) and they repress lateral root formation. In addition, auxin signaling acts downstream of SLs. AR formation is positively or negatively regulated by SLs depending largely on the plant species and experimental conditions. The relationship between SLs and auxin during AR formation appears to be complex. Most notably, this hormonal response is a key adaption that radically alters rice root architecture in response to nitrogen- and phosphate-deficient conditions.

Strigolactones (SLs) Regulate Root Development

Accumulating evidence indicates that SLs participate in root growth in many plant species. SLs promote the elongation of seminal/primary roots and adventitious roots (ARs)^1-4 and they repress lateral root (LR) formation.^1-3,5 In Arabidopsis, the length of the primary root in SL mutants was shown to be shorter than that in wild type plants due to a reduction in meristem cell number. This effect could be nullified by the application of GR24 (a synthetic and active SL) in wild-type and SL-deficient plants, but not in an SL-insensitive mutant.² Interestingly, in rice, SLs also positively control the elongation of ARs.^3-4 In the case of LR formation, LR density was shown to be increased in SL-deficient and -insensitive mutants of tomato,^2,6,7 while GR24 application decreased the LR density via the signaling gene MAX2, which suppresses LR outgrowth in Arabidopsis.² SLs positively or negatively regulate AR formation depending on the plant species and experimental conditions. For example, SLs act as suppressors of AR formation from non-root tissues.^8,9 AR formation was enhanced in SL mutants of Arabidopsis and pea and an examination of CYCLIN B1 expression suggested that SLs restrain the AR number by inhibiting the first formative divisions of founder cells.⁸ Conversely, Sun et al.¹⁰ found that rice SL mutants produced fewer ARs at the seedling stage and a lower number of ARs per tiller at the mature stage. The AR number in an SL synthetic mutant (d10), but not in an SL signaling mutant (d3), was complemented by GR24 application.

SLs participate in root development in response to nitrogen (N) and phosphate (P) deficiencies

N and P are major nutrients required for plant growth.^11,12 SLs play key roles in adaptive responses to N and P deficiencies due to elevated SL levels in roots.^13-17 For example, SLs promote symbioses with arbuscular mycorrhizal fungi by inducing hyphal branching and they adjust shoot architecture by inhibiting tiller bud outgrowth to better adapt to a P or N deficiency.^14,16-21 Recently, it was reported that SLs regulate the perception or response of plants to P-limited conditions.²² In Arabidopsis, mutants of SL signaling (max2-1) and biosynthesis (max4-1) showed reduced responses to P-limited conditions relative to wild-type plants. In max4-1, but not max2-1, the reduced response to low P was compensated by GR24 application. Moreover, abamineSG, which decreases SL levels in plants, reduced the response to low P in wild-type, but not in SL mutant, plants.²² Interestingly, several lines of evidence suggest that SLs are involved in rice root growth in response to N and P deficiencies.^3,4 The application of GR24 to wild-type plants and SL synthetic mutants, but not signaling mutants (d3), under nutrient-sufficient conditions led to the complete recovery of seminal root length and LR density compared to wild-type plants under N- and P-deficient conditions. This confirmed that elevated SL levels under nutrient-limiting conditions can lead to the D3-dependent induction of seminal root elongation and a reduction in LR density.⁴

Hormonal crosstalk between SLs and auxin during root development

In addition to SLs, auxins play a key role in establishing patterns of root morphology and are regulated by the levels of N and P.^4,23-25 In terms of seminal root and AR elongation and LR formation, based on an analysis of SL and auxin signaling mutants, it was found that auxin signaling acts downstream of SLs.^4,7,9,22 SLs may affect root growth via changes in auxin polar transport from shoot to root and/or auxin efflux in roots. Exogenous supplementation with GR24 interfered with PIN auxin-efflux carriers in roots,⁴ reducing the PIN1-GFP intensity in LR primordial.⁶ Thus, SLs might alter the level of auxin required for optimal root development and growth.² However, the relationship between SLs and auxin in regulating AR formation appears to be complex.^8,10 The positive effect of NAA (a synthetic auxin) application and the opposite effect of NPA (an auxin transport inhibitor) application on the AR number in wild-type plants suggests the importance of auxin for AR formation. Nevertheless, the AR number was still greater in wild-type plants compared to SL mutants, although they exhibited similar DR5::GUS expression levels regardless of the exogenous application of NAA or NPA.¹⁰ Similarly, SLs can at least partially reverse the stimulatory effect of auxin on adventitious rooting, and auxin can further increase the number of ARs in max mutants.⁸ At this stage, it is difficult to generalize about the interactions between SLs and auxin in AR formation.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Acknowledgment

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Funding

Research in China was funded by the National Natural Science Foundation, Innovative Research Team Development Plan of the Ministry of Education of China (No. IRT1256), the 111 Project (No. 12009), and PAPD Project.