A histidine kinase gene is required for large radius root tip circumnutation and surface exploration in rice

Kevin R Lehner, Isaiah Taylor, Erin N McCaskey, Rashmi Jain, Pamela C Ronald, Daniel I Goldman, Philip N Benfey

Preprint posted on 7 October 2018

Exploring the unseen: a putative histidine kinase promotes helical growth and soil surface exploration of rice roots

Selected by Martin Balcerowicz

Background: circumnutation – a long-known yet poorly understood growth phenotype in plants

The term circumnutation describes the helical growth of the tip of a plant organ. It is probably best known from tendrils of climbing plants such as grapevine or pea, but also occurs in various other plant organs including roots. This type of growth is considered to be the result of a complex interplay between an endogenous oscillator and external stimuli such as gravity and touch1, 2.

Circumnutation has been studied since the 19th century, when Darwin investigated helical growth patterns in various plant species3, but our understanding of its molecular basis is still rather limited. While several genes have been implicated in the control of shoot helical growth, the control of root tip circumnutation remains a black box. In their preprint, Lehner, Taylor et al. shed some light on this process as they identify a novel regulator of root tip circumnutation in rice, explore the signalling pathways involved and investigate a putative function of this process.

Key findings: OsHK1 enhances circumnutation of the root tip and promotes exploration of flat soil surfaces

The authors set out to identify genes involved in forming and structuring the rice root system by screening a mutant population for lines with altered root system architecture. They identified several mutants with increased primary root depth that harboured mutations in OsHK1, a gene encoding a putative histidine kinase. Imaging root growth at 15 min intervals for 2-3 days revealed that wild-type roots showed strong root tip circumnutation, which did not occur in the oshk1 mutant. The lack of this helical growth pattern likely caused the mutant’s deep root phenotype.

Another altered phenotype of oshk1 was observed when the root tip encountered a flat surface (such as a compacted soil layer): while the wild-type root kept growing directionally to “explore” the surface for pores or holes it can grow through, the oshk1 mutant root formed coils, thereby limiting the explored surface area. In their experiments the authors modelled this situation using plastic plates with small holes at different densities.  At low hole density, the oshk1 mutant was indeed less effective in finding these holes and thereby also in continuing to grow into deeper soil layers. Based on these observations, the authors hypothesise that root tip circumnutation is a mechanism to promote soil exploration and deeper growth through cracks or pores in dense soil layers.

The authors then went on to analyse the expression of OsHK1 in different organs by qPCR; OsHK1 exhibited strong expression in the root, with highest levels detected in the elongation zone, 1-2 mm above the root tip. Subsequent RNA-seq analysis on wild-type and mutant tissue spanning this area gave insight into the molecular consequences of an OsHK1 knock-out. Differentially expressed genes were enriched for GO terms related to the plant hormone cytokinin and also showed a strong overlap with previously reported cytokinin-regulated genes. Moreover, two additional observations link OsHK1 to cytokinin: firstly, the kinase encoded by OsHK1 appears to be structurally related to cytokinin receptors, although it lacks the actual cytokinin-binding domain; secondly, application of cytokinin rescued the abolished circumnutation phenotype of the oshk1 mutant. Taken together, these results suggest that OsHK1 promotes root tip circumnutation via activation of a cytokinin-related signalling pathway.

What I like about this preprint

I like that this preprint explores a seldom investigated, and thus somewhat obscure, phenotype. It does a very good job at presenting this phenotype through clear, concise graphs and stunning images and videos – I highly recommend to check them in the online supplementary material. I also found the experimental set-up to study the exploratory behaviour of roots, albeit its simplicity, quite intriguing.

Open questions

  • Does the oshk1 mutant display altered phenotypes in the shoot? Does oshk1 perform differently to wild type in terms of shoot growth or seed yield e.g. when grown in highly compacted soils?
  • Based on its sequence the OsHK1 protein is not likely to bind cytokinin, but is there any indication that expression of the OsHK1 gene is affected by cytokinin or any other endogenous or external signal?
  • The authors propose that the limited surface exploration of the oshk1 root is a result of its abolished root tip circumnutation. But is there a way to unambiguously show a causal relationship between these phenotypes and rule out that they are instead separate consequences of the loss of OsHK1 function?

References/Further reading

  1. Smyth, DR (2016). Helical growth in plant organs: mechanisms and significance. Development 143: 3272-3282
  2. Stolarz, M (2009). Circumnutation as a visible plant action and reaction. Physiological, cellular and molecular basis for circumnutations. Plant Signal. Behav. 4(5): 380–387
  3. Darwin, CR (1880). The power of movement in plants. London: John Murray.

Tags: cytokinin, histidine kinase, rice, root growth

Posted on: 5 November 2018


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