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In BriefIN BRIEF
Open Access

Nitrate Ahoy! Shoot Cytokinin Signals Integrate Growth Responses with Nitrogen Availability

Sonali Roy
Sonali Roy
Noble Research Institute Ardmore, Oklahoma
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  • For correspondence: sroy@noble.org

Published June 2018. DOI: https://doi.org/10.1105/tpc.18.00453

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  • © 2018 American Society of Plant Biologists. All rights reserved.

Nutrients are rarely distributed homogenously in soil. Consequently, plants have local and long-distance signaling systems in place to monitor and coordinate both demand and supply of essential macronutrients such as nitrogen (N). The “N-demand” long-distance signal emanates from a section of the root system that may be facing N deprivation, while the “N-supply” signal is activated if N has been found in the vicinity of the root. This allows the plant to adapt its root architecture and ensure optimal N supply by inducing the expression of hundreds of genes and increasing the number of lateral roots to forage for required nutrients (Kiba and Krapp, 2016).

Interestingly, this long-distance signal relay occurs systemically via the shoot. For example, xylem-mobile C-terminally encoded peptides produced in N-starved roots are components of the N-demand signaling pathway (Tabata et al., 2014); upon perception by their cognate receptors in shoots, they can induce nitrate uptake transporters in distal roots. Similarly, once imported, nitrate initiates root-to-shoot signaling involving biosynthesis and movement of the plant growth hormone cytokinin (CK) from the site of production in the roots to the shoots where they control N assimilation. Therefore, in heterogonous nitrate environments, nitrate-inducible IPT3 and IPT5 genes can affect overall plant development by controlling biosynthesis of different active forms of CK including trans-zeatin (Kieber and Schaller, 2014).

New results from Poitout et al. (2018) further push CK to the center stage of the systemic control of nitrate uptake and metabolism. The authors used a hydroponic split-root experimental system wherein Arabidopsis thaliana roots were partitioned into two compartments. These were set up in three combinations: both compartments containing the same media with nitrate (1 mM KNO3; N supplied homogenously), without nitrate (1 mM KCl; N deprived homogenously), or with each of these media in a different compartment (N supplied heterogeneously). Under these conditions, the authors compared the patterns of CK accumulation and associated transcriptional responses of the roots and shoots of wild-type plants to the CK biosynthetic and transport mutants ipt3,5,7 and abcg14, respectively. Importantly, impaired cytokinin biosynthesis and transport did not affect local nitrate perception. However, unlike the wild type, both mutants failed to display a characteristic induction of “sentinel” genes such as NITRITE REDUCTASE1 that respond rapidly to long-distance N-supply signals. Furthermore, transcriptomic analyses revealed that genes regulated by heterogeneous nitrate provision in shoots of wild-type plants were enriched for genes involved in glutamate synthesis, the amino acid into which N is first assimilated (Forde and Lea, 2007). By contrast, neither mutant showed this transcriptional reprogramming, indicating that N assimilation pathways in shoots are CK dependent. In parallel, the authors measured the levels of all four isoprenoid CK forms and their derivatives to correlate the transcriptional changes with CK accumulation patterns in roots and shoots. Curiously, in both mutants, only the reduced levels of trans-zeatin in shoots and not any of the other isoprenoid CK forms correlated with the dampened shoot transcriptional response. The authors concluded that shoot trans-zeatin controls downstream growth responses and further nitrate uptake and assimilation in response to heterogeneous nitrate availability (see figure).

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Model proposing the role of cytokinin in plant responses to heterogeneous nitrogen availability. NO3– provision leads to trans-zeatin (tZ) accumulation in roots, which is transported to the shoots and leads to differential control of root responses according to NO3– supply to the roots. The CK pathway is further integrated with the CEP-dependent pathway triggered in N-deprived roots. (Adapted from Poitout et al. [2018], Figure 6.)

Findings described in this study challenge existing theories on long-distance control of nitrogen uptake and form the basis of future work that will likely determine how cytokinin signaling networks are integrated with CEP signals associated with N foraging.

Footnotes

  • www.plantcell.org/cgi/doi/10.1105/tpc.18.00453

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References

  1. ↵
    1. Forde, B.G.,
    2. Lea, P.J.
    (2007). Glutamate in plants: metabolism, regulation, and signalling. J. Exp. Bot. 58: 2339–2358.
    OpenUrlCrossRefPubMed
  2. ↵
    1. Kiba, T.,
    2. Krapp, A.
    (2016). Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant Cell Physiol. 57: 707–714.
    OpenUrlCrossRefPubMed
  3. ↵
    1. Kieber, J.J.,
    2. Schaller, G.E.
    (2014). Cytokinins. The Arabidopsis Book 12: e0168, doi/10.1199/tab.0168.
    OpenUrl
  4. ↵
    1. Poitout, A.,
    2. Crabos, A.,
    3. Petřík, I.,
    4. Novák, O.,
    5. Krouk, G.,
    6. Lacombe, B.,
    7. Ruffel, S.
    (2018). Responses to systemic nitrogen signaling in Arabidopsis roots involve trans-zeatin in shoots. Plant Cell 30: 1243–1257.
    OpenUrlAbstract/FREE Full Text
  5. ↵
    1. Tabata, R.,
    2. Sumida, K.,
    3. Yoshii, T.,
    4. Ohyama, K.,
    5. Shinohara, H.,
    6. Matsubayashi, Y.
    (2014). Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346: 343–346.
    OpenUrlAbstract/FREE Full Text
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Nitrate Ahoy! Shoot Cytokinin Signals Integrate Growth Responses with Nitrogen Availability
Sonali Roy
The Plant Cell Jun 2018, 30 (6) 1169-1170; DOI: 10.1105/tpc.18.00453

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Nitrate Ahoy! Shoot Cytokinin Signals Integrate Growth Responses with Nitrogen Availability
Sonali Roy
The Plant Cell Jun 2018, 30 (6) 1169-1170; DOI: 10.1105/tpc.18.00453
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The Plant Cell: 30 (6)
The Plant Cell
Vol. 30, Issue 6
Jun 2018
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