CESA7 and microtubules pattern complex secondary cell walls in explosive fruit of Cardamine hirsuta

TL;DR

This study reveals how cellulose and microtubules shape specialized cell walls in the explosive seed pods of Cardamine hirsuta.

Contribution

The study identifies CESA7 and microtubules as key regulators of secondary cell wall patterning in explosive seed dispersal.

Findings

CESA7 is essential for cellulose synthesis in endb cells, influencing wall geometry and layering.

Cortical microtubules guide the deposition of cellulose, lignin, and xylan to form SCW-depleted domains.

Disrupting microtubules prevents the hinged geometry needed for explosive fruit coiling.

Abstract

Secondary cell walls (SCW) constitute the most abundant form of renewable plant biomass and are major sinks for atmospheric carbon. Their highly ordered patterns underpin specialized cell functions. In Cardamine hirsuta, the geometry of a polarly localized SCW in fruit endocarp b (endb) cells determines the mechanics of explosive seed dispersal. Yet, the genetic control of SCW synthesis and patterning in these specialized cells remains poorly understood. Here we show that CELLULOSE SYNTHASE 7 (CESA7) is required to synthesize SCW cellulose in endb cells. While lignin and xylan deposition occurs independently of cellulose patterning in cesa7 endb SCWs, the final geometry and layered organization of wild-type endb SCWs depend on CESA7. Cellulose serves as a scaffold for the organized assembly of SCW polymers, thereby maintaining the precise SCW patterns observed in endb cells of fruits and metaxylem cells in roots. Cortical microtubules guide the patterned deposition of cellulose, lignin and xylan in endb cells, creating SCW-depleted domains along cell edges that produce the specific hinged SCW geometry. Disrupting microtubules abolished this pattern and prevented explosive coiling of the fruit valves. Our findings show that microtubules and CESA7 shape the form and function of endb SCWs in exploding seed pods.

Spatial control of secondary cell wall synthesis and assembly establishes the wall geometry required for explosive seed dispersal in Cardamine hirsuta fruit.

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