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The expa1-1 mutant reveals a new biophysical lateral root organogenesis checkpoint

Priya Ramakrishna, Graham A. Rance, Lam D. Vu, Evan Murphy, Kamal Swarup, Kamaljit Moirangthem, Bodil Jorgensen, Brigitte van de Cotte, Tatsuaki Goh, Zhefeng Lin, Ute Voss, Tom Beeckman, Malcolm J. Bennett, Kris Gevaert, Ive De Smet

Preprint posted on January 18, 2018 https://www.biorxiv.org/content/early/2018/01/18/249961.1

How do plants decide where to place a new organ? This recent preprint on lateral root development provides new insights into a mechanical checkpoint and characterizes expa1-1 as a new player for the organization of asymmetric cell divisions.

Selected by Annika Weimer

Summary

How do plants decide where to place a new organ? This recent preprint on lateral root development provides new insights into a mechanical checkpoint and characterizes expa1-1 as new player for the organization of asymmetric cell divisions.

The bigger picture

One of the strategies plants use to increase the complexity of their root system is the continuous post-embryonic initiation of new lateral roots. Modulation of root architecture in general, and lateral root formation in particular, has profound impact on plant development, stress resistance and yield. Asymmetric cell divisions are crucial in various contexts during plant development and rigid cell walls prevents cells from moving. The local organization of division and differentiation is therefore indispensable for plant development. However, underlying mechanisms of asymmetric divisions remain scarce to date. Polarization cues from animals are not conserved and it is only recently that the plant field has started to assemble various pieces of the puzzle.

A new biophysical lateral root organogenesis checkpoint

Mechanical information provides important cues for cell polarity in uni- and multicellular systems. Underlying mechanisms in plant development, however, are not completely understood yet. Ramakrishna et al. compared transcriptomics data of genes induced by lateral root initiation with key regulators of asymmetric cell divisions and cell wall remodeling enzymes. They chose EXPANSIN A1 as a putative candidate. Pericycle cells locally bulge before asymmetric cell divisions which could be a result of local cell wall remodeling. EXPANSIN A1 shows a distinctive expression pattern in pericycle cells following nuclear migration before lateral roots emerge and it remains expressed in the small daughter cells after the formative division. The expa1-1 mutant displays auxin-dependent differences in the biochemical properties of pericycle cell walls which affects local bulging required for proper positioning of the cell division plane. Strikingly, the expa1-1 mutant loses the organized cell pattern during early stages of lateral root initiation seen in wild-type plants. The authors suggest a new biophysical lateral root organogenesis checkpoint that depends on pericycle cell width.

Future perspective

  • EXPANSIN A1 appears to locally induce cell wall remodeling in pericycle cells. This suggest a polarity cue that either directly or indirectly regulates EXPANSIN A1 action in only parts of the cell.
  • Asymmetric cell divisions still occur in expa1-1 mutants, however they are oddly positioned, which hints at factors for the establishment of cortical division plane determination downstream of EXPANSIN A1.
  • The Arabidopsis genome encodes for many expansins. Given the relatively mild phenotype of expa1-1, how redundant are the homologues and do those also play a role during formative divisions. And if so, where?
  • How does auxin regulate the local action of EXPANSIN A1 in pericycle cells?
  • Is EXPANSIN A1 also expressed in other parts of the plant? How many days after germination was the expression of EXPANSIN A1 quantified and how many lateral roots are present at that time? Does it play a similar role during other formative divisions or in completely different contexts?

Figure: A minimum width is required for ordered asymmetric divisions of founder cells during lateral root initiation. If the whole pericycle bulges, as in the expa1-1 mutant, asymmetric cell divisions do not occur in a coordinated way. Figure taken from Fig. 4E of the original preprint.

Tags: arabidopsis, asymmetric cell divisions, cell wall remodeling, expansin, lateral roots, plant development

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  • Author's response

    Ive De Smet shared

    EXPANSIN loss-of-function phenotypes are scarce, so we were extremely enthusiastic when our detailed microscopic analyses revealed a developmental defect in the expa1-1 mutant. This work will be the starting point to explore local auxin action, polarity cues and division plane positioning in the pericycle.
    Regarding some of the questions you raised, I have the following reply.
    Is EXPANSIN A1 also expressed in other parts of the plant?  Interestingly, EXPA1 is also expressed in Arabidopsis guard cells and seems to control stomatal opening (Zhang et al 2001 Plant Cell Rep 30:27-36).
    Does it play a similar role during other formative divisions or in completely different contexts? More detailed studies will reveal if EXPA1 is expressed during and plays a role in, for example, (early) stomata development.
    How many days after germination was the expression of EXPANSIN A1 quantified?  EXPA1expression was analyzed in seedling roots 5 days after germination.

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