Hydropatterning—how roots test the waters

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As sessile organisms, plants rely on their roots to acquire sufficient water and nutrients from the soil. Making the right choice about where to deploy new roots can determine survival, especially when soil resources are scarce and unevenly distributed. Recently, it was discovered that plant roots can respond to gradients of soil moisture by favoring the formation of lateral roots toward sites with available water ([ 1 ][1]). On page 1407 of this issue, Orosa-Puente et al. ([ 2 ][2]) show how growth along an air-water interface in the soil triggers asymmetric activation of a signaling module coordinated by the plant hormone auxin that biases lateral root initiation to the side in contact with water. These findings demonstrate how spatial environmental cues determine organ formation in higher plants.

The ability to generate new roots postembryonically confers plants a high degree of developmental plasticity. The formation of lateral roots starts deep in the parental root tissue. There, a specific number of cells of the pericycle, the tissue that delimits the root vasculature, are “primed” as lateral root founder cells at periodic intervals ([ 3 ][3]). Rather than progressing continuously, the initiation of lateral roots from primed pericycle cells can be stimulated or arrested at any developmental stage ([ 4 ][4]), allowing roots to adjust the number and spacing of lateral roots to the prevailing environmental conditions. This plasticity offers plants the opportunity to efficiently colonize regions of high resource availability, as long as root sensing mechanisms can precisely locate these sites.

In many plant species, low water availability can stimulate root expansion and steeper growth angles to improve water uptake from deeper soil layers ([ 5 ][5], [ 6 ][6]). In soils that are not completely dry or flooded, an airwater interface develops between soil particles (see the figure). At this microscale, variations in water availability trigger abscisic acid–dependent hydrotropic growth to differentially modulate cell elongation, allowing roots to bend toward water ([ 7 ][7], [ 8 ][8]). Additionally, tissue patterning is altered when roots are exposed to differential water availability on either side of the root. This adaptive response, termed hydropatterning, induces the formation of root hairs and aerenchyma (plant tissues containing enlarged gas-filled intercellular spaces) in the air-exposed side of roots, while positioning more lateral roots on the side that has direct contact with water ([ 1 ][1]). Although local water availability induces auxin biosynthesis and signaling ([ 1 ][1]), it has remained unknown how these changes are translated into asymmetrical lateral root formation across the root axis.

![Figure][9]

Shaped by water
Where there are small-scale differences in water availability around soil particles, water potential gradients are sensed in roots (red cells). Hydrotropism guides roots towards water, whereas hydropatterning alters the distribution of root hairs and lateral roots along the root circumference (not to scale). ARF7-dependent asymmetric LBD16 expression triggers lateral root initiation on the side in contact with water.

GRAPHIC: N. DESAI/ SCIENCE

Orosa-Puente et al. found that mutations in the transcription factor AUXIN RESPONSE FACTOR 7 (ARF7), a key regulator of lateral root initiation ([ 9 ][10]), impaired the ability of plants to bias root branching toward moisture. Although LATERAL ORGAN BOUNDARIES-DOMAIN 16 (LBD16), a downstream target of ARF7, accumulates preferentially in lateral root founder cells on the water-exposed side, ARF7 is evenly expressed around the circumferential axis of the root. However, ARF7 can be posttranslationally modified with small ubiquitin modifier (SUMO). Arabidopsis plants lacking the SUMO proteases OVERLY TOLERANT TO SALT 1 (OTS1) and OTS2 ([ 10 ][11]), which promote deconjugation of SUMO from ARF7, exhibit a hydropatterning defect akin to ARF7 mutants. Intriguingly, SUMOylation does not affect the universal function of ARF7 to promote lateral root initiation but instead affects its capability to regulate the root branching pattern in response to water. ARF proteins can be inactivated by INDOLE-3-ACETIC ACID–INDUCIBLE (IAA) proteins in an auxin-dependent manner ([ 11 ][12]). This is also the case for ARF7, the DNA-binding activity of which is controlled by IAA3 and IAA14 at different stages of lateral root development ([ 12 ][13], [ 13 ][14]). Orosa-Puente et al. identified that SUMOylation is specifically required for ARF7 recruitment and inactivation by IAA3 but is dispensable for the interaction with IAA14. These findings provide insights into how an environmental cue can fine-tune the function of common regulators of development to induce specific phenotypic plasticity.

Hydropatterning is conserved in many plant species and targets early stages of lateral root development, such as the positioning of founder cells along the main root axis ([ 1 ][1]). Developmental competence for hydropatterning is largely limited to the root zone undergoing active growth and is lost as cells mature ([ 14 ][15]). This has led to the hypothesis that water gradients are sensed near the root tip, leaving a positional imprint that triggers lateral root initiation further up in the root. In the growing root tip, cell expansion builds up a water potential gradient that increases hydraulic conductivity ([ 14 ][15]). As water uptake rates are higher in expanding cells, differential access to water along the root circumference may generate sizable differences in water potential. Yet, experimentally demonstrating the existence of such gradients at this scale is very challenging. More research is necessary to uncover how root cells sense water potentials and how signals detected in outer cells are transmitted to inner root tissue. Interestingly, Orosa-Puente et al. observed that ARF7 SUMOylation occurs when roots are exposed to air, even though they have been unable to demonstrate if ARF7 is differentially SUMOylated in a root exposed to an air-water interface. Nonetheless, this finding suggests that the absence of water on its own serves as an informative cue for developmental decisions without depending on changes in cellular osmolarity.

Because water is such a critical resource for plant growth and development, it is not surprising that plants have evolved additional adaptive mechanisms. Although hydropatterning can increase root surface contact with water, the steering of growth direction by hydrotropism places this organ in water-available sites. Thus, if lateral roots primed by hydropatterning emerge at sites that become dry, hydrotropic growth allows them to maneuver toward water.

Considering the strong negative impact of precipitation variability on crop yield ([ 15 ][16]), breeding crops with a predefined root system architecture may be less appropriate than exploiting plasticity and sensing mechanisms to improve root adaptability to spatial and temporal variations of soil moisture. In this context, it will be interesting to determine the contribution of hydropatterning to water and nutrient uptake under challenging water regimes and to investigate how water and nutrient signals are integrated to shape root system architecture. Thus, manipulating the molecular mechanism uncovered by Orosa-Puente et al. and tapping into possible natural allelic variation for hydropatterning have potential for breeding crops that are better able to withstand environmental stresses.

1. [↵][17]1. Y. Bao et al

., Proc. Natl. Acad. Sci. U.S.A. 111, 9319 (2014).

[OpenUrl][18][Abstract/FREE Full Text][19]

2. [↵][20]1. B. Orosa-Puente et al

., Science 362, 1407 (2018).

[OpenUrl][21][Abstract/FREE Full Text][22]

3. [↵][23]1. M. A. Moreno-Risueno et al

., Science 329, 1306 (2010).

[OpenUrl][24][Abstract/FREE Full Text][25]

4. [↵][26]1. J. Lavenus et al

., Trends Plant Sci. 18, 450 (2013).

[OpenUrl][27][CrossRef][28][PubMed][29]

5. [↵][30]1. Y. Uga et al

., Nat. Genet. 45, 1097 (2013).

[OpenUrl][31][CrossRef][32][PubMed][33]

6. [↵][34]1. R. Rellán-Álvarez et al

., eLife 4, e07597 (2015).

[OpenUrl][35][CrossRef][36]

7. [↵][37]1. N. Takahashi et al

., Planta 216, 203 (2002).

[OpenUrl][38][CrossRef][39][PubMed][40][Web of Science][41]

8. [↵][42]1. D. Dietrich et al

., Nat. Plants 3, 17057 (2017).

[OpenUrl][43]

9. [↵][44]1. Y. Okushima et al

., Plant Cell 19, 118 (2007).

[OpenUrl][45][Abstract/FREE Full Text][46]

10. [↵][47]1. L. Conti et al

., Plant Cell 20, 2894 (2008).

[OpenUrl][48][Abstract/FREE Full Text][49]

11. [↵][50]1. S. B. Tiwari et al

., Plant Cell 16, 533 (2004).

[OpenUrl][51][Abstract/FREE Full Text][52]

12. [↵][53]1. H. Fukaku et al

., Plant J. 44, 382 (2005).

[OpenUrl][54][CrossRef][55][PubMed][56][Web of Science][57]

13. [↵][58]1. K. Swarup et al

., Nat. Cell Biol. 10, 946 (2008).

[OpenUrl][59][CrossRef][60][PubMed][61][Web of Science][62]

14. [↵][63]1. N. E. Robins II,
2. J. R. Dinneny

, Proc. Natl. Acad. Sci. U.S.A. 115, E822 (2018).

[OpenUrl][64][Abstract/FREE Full Text][65]

15. [↵][66]1. D. K. Ray et al

., Nat. Commun. 6, 5989 (2015).

[OpenUrl][67][CrossRef][68]

[1]: #ref-1
[2]: #ref-2
[3]: #ref-3
[4]: #ref-4
[5]: #ref-5
[6]: #ref-6
[7]: #ref-7
[8]: #ref-8
[9]: pending:yes
[10]: #ref-9
[11]: #ref-10
[12]: #ref-11
[13]: #ref-12
[14]: #ref-13
[15]: #ref-14
[16]: #ref-15
[17]: #xref-ref-1-1 “View reference 1 in text”
[18]: {openurl}?query=rft.jtitle%253DProc.%2BNatl.%2BAcad.%2BSci.%2BU.S.A.%26rft_id%253Dinfo%253Adoi%252F10.1073%252Fpnas.1400966111%26rft_id%253Dinfo%253Apmid%252F24927545%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[19]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6NDoicG5hcyI7czo1OiJyZXNpZCI7czoxMToiMTExLzI1LzkzMTkiO3M6NDoiYXRvbSI7czoyMzoiL3NjaS8zNjIvNjQyMS8xMzU4LmF0b20iO31zOjg6ImZyYWdtZW50IjtzOjA6IiI7fQ==
[20]: #xref-ref-2-1 “View reference 2 in text”
[21]: {openurl}?query=rft.jtitle%253DScience%26rft.stitle%253DScience%26rft.aulast%253DOrosa-Puente%26rft.auinit1%253DB.%26rft.volume%253D362%26rft.issue%253D6421%26rft.spage%253D1407%26rft.epage%253D1410%26rft.atitle%253DRoot%2Bbranching%2Btoward%2Bwater%2Binvolves%2Bposttranslational%2Bmodification%2Bof%2Btranscription%2Bfactor%2BARF7%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscience.aau3956%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[22]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6Mzoic2NpIjtzOjU6InJlc2lkIjtzOjEzOiIzNjIvNjQyMS8xNDA3IjtzOjQ6ImF0b20iO3M6MjM6Ii9zY2kvMzYyLzY0MjEvMTM1OC5hdG9tIjt9czo4OiJmcmFnbWVudCI7czowOiIiO30=
[23]: #xref-ref-3-1 “View reference 3 in text”
[24]: {openurl}?query=rft.jtitle%253DScience%26rft.stitle%253DScience%26rft.aulast%253DMoreno-Risueno%26rft.auinit1%253DM.%2BA.%26rft.volume%253D329%26rft.issue%253D5997%26rft.spage%253D1306%26rft.epage%253D1311%26rft.atitle%253DOscillating%2BGene%2BExpression%2BDetermines%2BCompetence%2Bfor%2BPeriodic%2BArabidopsis%2BRoot%2BBranching%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscience.1191937%26rft_id%253Dinfo%253Apmid%252F20829477%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[25]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6Mzoic2NpIjtzOjU6InJlc2lkIjtzOjEzOiIzMjkvNTk5Ny8xMzA2IjtzOjQ6ImF0b20iO3M6MjM6Ii9zY2kvMzYyLzY0MjEvMTM1OC5hdG9tIjt9czo4OiJmcmFnbWVudCI7czowOiIiO30=
[26]: #xref-ref-4-1 “View reference 4 in text”
[27]: {openurl}?query=rft.jtitle%253DTrends%2BPlant%2BSci.%26rft.volume%253D18%26rft.spage%253D450%26rft_id%253Dinfo%253Adoi%252F10.1016%252Fj.tplants.2013.04.006%26rft_id%253Dinfo%253Apmid%252F23701908%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[28]: /lookup/external-ref?access_num=10.1016/j.tplants.2013.04.006&link_type=DOI
[29]: /lookup/external-ref?access_num=23701908&link_type=MED&atom=%2Fsci%2F362%2F6421%2F1358.atom
[30]: #xref-ref-5-1 “View reference 5 in text”
[31]: {openurl}?query=rft.jtitle%253DNat.%2BGenet.%26rft.volume%253D45%26rft.spage%253D1097%26rft_id%253Dinfo%253Adoi%252F10.1038%252Fng.2725%26rft_id%253Dinfo%253Apmid%252F23913002%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[32]: /lookup/external-ref?access_num=10.1038/ng.2725&link_type=DOI
[33]: /lookup/external-ref?access_num=23913002&link_type=MED&atom=%2Fsci%2F362%2F6421%2F1358.atom
[34]: #xref-ref-6-1 “View reference 6 in text”
[35]: {openurl}?query=rft.jtitle%253DeLife%26rft_id%253Dinfo%253Adoi%252F10.7554%252FeLife.07597%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[36]: /lookup/external-ref?access_num=10.7554/eLife.07597&link_type=DOI
[37]: #xref-ref-7-1 “View reference 7 in text”
[38]: {openurl}?query=rft.jtitle%253DPlanta%26rft.stitle%253DPlanta%26rft.aulast%253DTakahashi%26rft.auinit1%253DN.%26rft.volume%253D216%26rft.issue%253D2%26rft.spage%253D203%26rft.epage%253D211%26rft.atitle%253DHydrotropism%2Bin%2Babscisic%2Bacid%252C%2Bwavy%252C%2Band%2Bgravitropic%2Bmutants%2Bof%2BArabidopsis%2Bthaliana.%26rft_id%253Dinfo%253Adoi%252F10.1007%252Fs00425-002-0840-3%26rft_id%253Dinfo%253Apmid%252F12447533%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[39]: /lookup/external-ref?access_num=10.1007/s00425-002-0840-3&link_type=DOI
[40]: /lookup/external-ref?access_num=12447533&link_type=MED&atom=%2Fsci%2F362%2F6421%2F1358.atom
[41]: /lookup/external-ref?access_num=000180037300002&link_type=ISI
[42]: #xref-ref-8-1 “View reference 8 in text”
[43]: {openurl}?query=rft.jtitle%253DNat.%2BPlants%26rft.volume%253D3%26rft.spage%253D17057%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[44]: #xref-ref-9-1 “View reference 9 in text”
[45]: {openurl}?query=rft.jtitle%253DPlant%2BCell%26rft_id%253Dinfo%253Adoi%252F10.1105%252Ftpc.106.047761%26rft_id%253Dinfo%253Apmid%252F17259263%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
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[47]: #xref-ref-10-1 “View reference 10 in text”
[48]: {openurl}?query=rft.jtitle%253DPlant%2BCell%26rft_id%253Dinfo%253Adoi%252F10.1105%252Ftpc.108.058669%26rft_id%253Dinfo%253Apmid%252F18849491%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
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[50]: #xref-ref-11-1 “View reference 11 in text”
[51]: {openurl}?query=rft.jtitle%253DPlant%2BCell%26rft_id%253Dinfo%253Adoi%252F10.1105%252Ftpc.017384%26rft_id%253Dinfo%253Apmid%252F14742873%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
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[53]: #xref-ref-12-1 “View reference 12 in text”
[54]: {openurl}?query=rft.jtitle%253DThe%2BPlant%2Bjournal%2B%253A%2B%2Bfor%2Bcell%2Band%2Bmolecular%2Bbiology%26rft.stitle%253DPlant%2BJ%26rft.aulast%253DFukaki%26rft.auinit1%253DH.%26rft.volume%253D44%26rft.issue%253D3%26rft.spage%253D382%26rft.epage%253D395%26rft.atitle%253DTissue-specific%2Bexpression%2Bof%2Bstabilized%2BSOLITARY-ROOT%252FIAA14%2Balters%2Blateral%2Broot%2Bdevelopment%2Bin%2BArabidopsis.%26rft_id%253Dinfo%253Adoi%252F10.1111%252Fj.1365-313X.2005.02537.x%26rft_id%253Dinfo%253Apmid%252F16236149%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[55]: /lookup/external-ref?access_num=10.1111/j.1365-313X.2005.02537.x&link_type=DOI
[56]: /lookup/external-ref?access_num=16236149&link_type=MED&atom=%2Fsci%2F362%2F6421%2F1358.atom
[57]: /lookup/external-ref?access_num=000232660000003&link_type=ISI
[58]: #xref-ref-13-1 “View reference 13 in text”
[59]: {openurl}?query=rft.jtitle%253DNature%2BCell%2BBiology%26rft.stitle%253DNature%2BCell%2BBiology%26rft.aulast%253DSwarup%26rft.auinit1%253DK.%26rft.volume%253D10%26rft.issue%253D8%26rft.spage%253D946%26rft.epage%253D954%26rft.atitle%253DThe%2Bauxin%2Binflux%2Bcarrier%2BLAX3%2Bpromotes%2Blateral%2Broot%2Bemergence.%26rft_id%253Dinfo%253Adoi%252F10.1038%252Fncb1754%26rft_id%253Dinfo%253Apmid%252F18622388%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[60]: /lookup/external-ref?access_num=10.1038/ncb1754&link_type=DOI
[61]: /lookup/external-ref?access_num=18622388&link_type=MED&atom=%2Fsci%2F362%2F6421%2F1358.atom
[62]: /lookup/external-ref?access_num=000258147100012&link_type=ISI
[63]: #xref-ref-14-1 “View reference 14 in text”
[64]: {openurl}?query=rft.jtitle%253DProc.%2BNatl.%2BAcad.%2BSci.%2BU.S.A.%26rft_id%253Dinfo%253Adoi%252F10.1073%252Fpnas.1710709115%26rft_id%253Dinfo%253Apmid%252F29317538%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[65]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6NDoicG5hcyI7czo1OiJyZXNpZCI7czoxMDoiMTE1LzQvRTgyMiI7czo0OiJhdG9tIjtzOjIzOiIvc2NpLzM2Mi82NDIxLzEzNTguYXRvbSI7fXM6ODoiZnJhZ21lbnQiO3M6MDoiIjt9
[66]: #xref-ref-15-1 “View reference 15 in text”
[67]: {openurl}?query=rft.jtitle%253DNat.%2BCommun.%26rft.volume%253D6%26rft.spage%253D5989%26rft_id%253Dinfo%253Adoi%252F10.1038%252Fncomms6989%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[68]: /lookup/external-ref?access_num=10.1038/ncomms6989&link_type=DOI

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