Strigolactones repress nodule development and senescence in pea

Abstract

SUMMARYStrigolactones are a class of phytohormones that are involved in many different plant developmental processes, including the rhizobium–legume nodule symbiosis. Although both positive and negative effects of strigolactones on the number of nodules have been reported, the influence of strigolactones on nodule development is still unknown. Here, by means of the ramosus (rms) mutants of Pisum sativum (pea) cv Terese, we investigated the impact of strigolactone biosynthesis (rms1 and rms5) and signaling (rms3 and rms4) mutants on nodule growth. The rms mutants had more red, that is, functional, and larger nodules than the wild‐type plants. Additionally, the increased nitrogen fixation and senescence zones with consequently reduced meristematic and infection zones indicated that the rms nodules developed faster than the wild‐type nodules. An enhanced expression of the nodule zone‐specific molecular markers for meristem activity and senescence supported the enlarged, fast maturing nodules. Interestingly, the master nodulation regulator, NODULE INCEPTION, NIN, was strongly induced in nodules of all rms mutants but not prior to inoculation. Determination of sugar levels with both bulk and spatial metabolomics in roots and nodules, respectively, hints at slightly increased malic acid levels early during nodule primordia formation and reduced sugar levels at later stages, possibly the consequence of an increased carbon usage of the enlarged nodules, contributing to the enhanced senescence. Taken together, these results suggest that strigolactones regulate the development of nodules, which is probably mediated through NIN, and available plant sugars.

Perception of butenolides byBacillus subtilisvia the α/β-hydrolase RsbQ

“…Strigolactones exuded by pea roots promote nodulation with R. leguminosarum , most probably by acting on the bacterial partner 43 . However, a recent study on pea but with a different bacterial strain reached a contradictory conclusion in which strigolactones appeared to repress nodule development and maturation 44 . There is also potential for butenolide signals derived from bacteria: for example, Streptomyces albus J10764 secretes a series of desmethyl butenolides that can stimulate interspecific secondary metabolism in S. avermitilis 45 , and at least one of these compounds can promote seed germination of the parasitic weed Orobanche minor 46 .…”

Signaling in Legume–Rhizobia Symbiosis

“…Not less importantly, NIN was reported to enhance the expression of CLAV-ATA3/Embryo-surrounding region-related peptides (CLE, Figure 4), which are known to be the signals that suppress nodulation [128,135]. Thus, these peptides are involved in regulation of nodule formation and impact on the nodulation efficiency.…”

“…Thus, the role of GR24 in the delay of the nodule development and senescence was shown. Moreover, these effects are most likely mediated by NIN and available plant sugars [135].…”

Pushing pea: fine‐tuning of nodule development by strigolactones

“…Pea is unique amongst the legumes because there is a range of well-characterised strigolactone-biosynthesis and response mutants available (Beveridge et al, 1996). For the highlighted publication, Van Dingenen, Goormachtig and colleagues therefore set out to analyse the impact of strigolactone biosynthesis and signalling on nodule development in pea (Van Dingenen et al, 2023).…”

“…The authors speculate that the opposing results of the effect of strigolactone during nodulation in different plant species might be explained by the different time points used to examine the nodules. Some studies use a very early time point, i.e., 9 days after inoculation with rhizobia (Foo et al, 2013), whereas Van Dingenen et al (2023) analysed the influence of strigolactones on nodule development at later stages, at 4 weeks after inoculation. Moreover, strigolactones tightly interact with other phytohormones such as auxins and cytokinins (Hayward et al, 2009).…”