Sandra Isabel González-Morales, Ricardo A. Chávez-Montes, Corina Hayano-Kanashiro, Gerardo Alejo-Jacuinde, Thelma Y. Rico-Cambron, Stefan de Folter, and Luis Herrera-Estrella

Significance

Seed desiccation tolerance (DT) is one of the most fascinating processes of higher plants, and has played a fundamental role in the evolution of land plants. DT allows plant seeds to remain viable in the dry state for years and even centuries. What the key transcription factors (TFs) are that activate the mechanisms that allow plant seeds to maintain cellular and DNA integrity for centuries remains largely unknown. In this paper, we report the identification of the TFs that act as major nodes of the transcriptional networks that regulate the acquisition of seed DT. We also report the functional validation of several of the major regulators of seed DT in plants.

Abstract

Desiccation tolerance (DT) is a remarkable process that allows seeds in the dry state to remain viable for long periods of time that in some instances exceed 1,000 y. It has been postulated that seed DT evolved by rewiring the regulatory and signaling networks that controlled vegetative DT, which itself emerged as a crucial adaptive trait of early land plants. Understanding the networks that regulate seed desiccation tolerance in model plant systems would provide the tools to understand an evolutionary process that played a crucial role in the diversification of flowering plants. In this work, we used an integrated approach that included genomics, bioinformatics, metabolomics, and molecular genetics to identify and validate molecular networks that control the acquisition of DT in Arabidopsis seeds. Two DT-specific transcriptional subnetworks were identified related to storage of reserve compounds and cellular protection mechanisms that act downstream of the embryo development master regulators LEAFY COTYLEDON 1 and 2, FUSCA 3, and ABSCICIC ACID INSENSITIVE 3. Among the transcription factors identified as major nodes in the DT regulatory subnetworks, PLATZ1, PLATZ2, and AGL67 were confirmed by knockout mutants and overexpression in a desiccation-intolerant mutant background to play an important role in seed DT. Additionally, we found that constitutive expression of PLATZ1 in WT plants confers partial DT in vegetative tissues.

See: http://www.pnas.org/content/113/35/E5232.abstract.html?etoc

PNAS 30 2016; Vol. 113; no.35: E5232–E5241

Fig. 1.

Global gene expression profile in seed desiccation-intolerant mutants. (A) Heat map from hierarchical clustering of differentially expressed genes. Each mutant was compared with its corresponding wild type (lec1-1 and lec2-1 versus Ws; abi3-5 versus Ler; fus3-3 versus Col-0) at three developmental stages, 15, 17, and 21 DAF. Green indicates down-regulated values, red indicates up-regulated values, and black indicates unchanged values. The yellow rectangles indicate the common down-regulated genes between intolerant mutants. DI, desiccation-intolerant; DT, desiccation-tolerant. (B) Venn diagrams showing the number and distribution of differential genes across the comparison among mutants representing down-regulated genes at 15, 17, and 21 DAF. Genes potentially related to desiccation tolerance are indicated in red.