Gravitropisms and reaction woods of forest trees – evolution, functions and mechanisms

Abstract

Summary The woody stems of trees perceive gravity to determine their orientation, and can produce reaction woods to reinforce or change their position. Together, graviperception and reaction woods play fundamental roles in tree architecture, posture control, and reorientation of stems displaced by wind or other environmental forces. Angiosperms and gymnosperms have evolved strikingly different types of reaction wood. Tension wood of angiosperms creates strong tensile force to pull stems upward, while compression wood of gymnosperms creates compressive force to push stems upward. In this review, the general features and evolution of tension wood and compression wood are presented, along with descriptions of how gravitropisms and reaction woods contribute to the survival and morphology of trees. An overview is presented of the molecular and genetic mechanisms underlying graviperception, initial graviresponse and the regulation of tension wood development in the model angiosperm, Populus. Critical research questions and new approaches are discussed.

Transcriptional and temporal response of Populus stems to gravi‐stimulation

“…Results from this analysis show that tension wood expression from clusters 10, 11 and 13 were highly correlated with the rate of gravibending but not normalized lift (Table S3) and suggests that a subset of genes (385, 511, 529 genes respectively) may be directly involved in tension wood formation. These clusters contain numerous genes that have previously been implicated in wood formation processes (Zhong et al ; Hussey et al ; Nakano et al ; Ye and Zhong ; Groover ) and provide insight into genes may be directly involved in tension wood specific processes such as increase rate of cell division, cell differentiation, and the formation and maturation of the gelatinous cell wall layer (Andersson‐Gunnerås et al ; Mellerowicz and Gorshkova ; Gerttula et al ). For example, these clusters contained genes that have been characterized as major regulators of wood formation (ARK1 (Potri.004G004700), BEL1 (Potri.003G131300), GATA12 (Potri.006G237700), KNAT7 (Potri.001G112200), MYB4 (Potri.004G174400, Potri.009G134000), MYB42 (Potri.001G118800), MYB85 (Potri.015G129100), MYB103 (Potri.001G099800, Potri.003G132000), WOX13 (Potri.005G101800, Potri.005G252800)), structural genes involved in secondary cell wall formation (CESA (Potri.001G266400, Potri.002G066600, Potri.004G059600, Potri.005G087500, Potri.006G052600, Potri.007G076500, Potri.009G060800, Potri.011G069600, Potri.016G054900, Potri.018G029400), COBL4 (Potri.004G117200), IRX10 (Potri.001G068100), LAC17 (Potri.006G087100, Potri.006G087500) and tension wood formation (PtFLA6, FLA11‐like, FLA12‐like, xyloglucan endotransglycosylase).…”

“…Most angiosperm trees respond to external forces including gravity, wind, and snow loading through the production of specialized tension wood fibers to reinforce and reorient the lignified portion of stems and branches (Ruelle et al ; Groover ). For example, Populus trees subjected to a 90° gravi‐stimulation treatment reorient the lignified portion of the stem against the gravity vector (gravibending) (Figure A).…”

Plant ‘muscles’: fibers with a tertiary cell wall

“…Although gelatinous fibers are found in different taxonomic groups, they predominate in angiosperm plants. The best‐known example of fibers with a tertiary cell wall is G‐fibers of tension wood (Mellerowicz & Gorshkova, ; Alméras & Clair, ; Groover, ). However, based on compositional and architectural similarity, it appears that G‐fibers are not exclusive to trees and to xylem cell types (Gorshkova et al ., ; Tomlinson et al ., ).…”

Ethylene signaling induces gelatinous layers with typical features of tension wood in hybrid aspen

“…Tension wood (TW) is formed on one side of a stem or a branch of angiosperm trees upon displacement resulting from, for example, bending or leaning. TW induces tensional stress in the wood that reorients the branch/stem towards its original position (Mellerowicz & Gorshkova, ; Felten & Sundberg, ; Fagerstedt et al ., ; Fournier et al ., ; Ruelle, ; Groover, ). TW is associated with an asymmetric cambial growth of the stem/branch, decreased size and frequency of vessels, and a change in the ultrastructure and chemistry of the fiber cell wall.…”