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NCBS team identifies a tiny molecule in rice that facilitated domestication from wild grass

The grains we eat, the flowers we cherish, fruits that we use as supplements, all came from plants that have been extensively modified from their original forms in a process called domestication.  Domestication of plants and animals has been the subject of fascinating studies over the last many decades.  Domestication encompasses a broad spectrum of evolutionary changes called as “domestication syndrome” that distinguish most crops from their progenitors.  These changes may increase fitness of these plants under ideal man-made conditions, but likely decrease their fitness in the wild.  Complete dependence on humans for survival of domesticated crops can be considered as the fulfilment of domestication.  Maize and brassicas such as cauliflower are examples of such highly modified forms.

Indica rice that most of us eat almost every day, was domesticated from two wild plants namely, Oryza nivara and O. rufipogon, in South and East Asia.  Both these wild grass species are still found in many rice-growing areas, often growing wild next to cultivated areas, edges of lakes and field-bunds.  Some of these wild accessions are perennial and often have long prostrate habits.  Domestication of rice involved incorporation of specific yield-related changes in wild species of rice.  The rice domestication selected key traits (or useful change) such as absence of seed shattering (that now allows mature seed to stay in the plants), breaking of seed dormancy, plant architecture, number of grains per plant, tolerance to stresses and diseases, and grain color, nutrients and/or aroma.

The recent advances in genomics have provided new tools to investigate the genetic basis and consequences of rice domestication.  In the genomic era, numerous genes that are responsible for rice domestication have been identified. Predictably, these included genes with functions for control of transcription (ability to induce making of RNA from other genes), transportation of cargo, modulation of hormonal activities and metabolic regulators.  However, surprisingly, it was learnt that phenotypic diversity of domesticated crops are not proportional to genomic changes (variations in DNA sequence).  This has promoted several lines of enquiry into possibilities of other causes (other than changes in DNA sequence) that might have contributed to phenotypic changes associated with domestication.  It was widely speculated that regulatory molecules named small (s)RNAs might contribute towards domestication-associated changes by altering ability to control production of specific proteins. sRNAs are tiny messengers that dictate which genes can make proteins, often at specific times and specific locations within the organism.

By comparing sRNA populations of wild species of indica rice, hundreds of landraces (rice varieties that were grown until green revolution) and cultivated high-yielding rice lines, our laboratory at NCBS has identified one specific sRNA that regulates multiple aspects of rice growth and development.  While this sRNA is expressed at high levels in wild species of rice, it was shut-off gradually to improve mechanical strength of rice stems through altered lignification. Lignin provides mechanical strength and more lignin means sturdy plants that can bear many seeds. This is logical since wild species of rice were prostrate forms, dwelling in semi-aquatic systems, rarely requiring stronger stems.  The sRNA and the genes it regulates are hidden reasons behind at least 26 genomic regions (QTL) previously implicated in rice yield.  Our analyses suggest that such a strategy is a likely contributor to domestication-associated phenotypes if crops had evolved from semi-aquatic wild progenitors.  A direct application of this finding is to use it as a molecular marker for breeding of high yielding rice varieties.

‘The most important finding of our study is that when rice accumulates increased levels of lignin, it gives additional strength to the plant to bear more grains. Our finding gives an opportunity to our breeders to efficiently improve the rice yield by reducing miR397 or by elevating laccase levels’ said Swetha Chenna, first author of the paper that appeared in the Plant Cell as ‘Breakthrough Report’.

‘Understanding mechanisms that contributed to crop yield is undoubtedly a key area for plant biology. With the identification of first such non-genic regulator in crop domestication, we hope that future research unravels other changes associated with domestication of plants (and animals), spearheading further improvement in crops for the future’ felt Dr. Padubidri V. Shivaprasad, a group leader at National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore.  His laboratory is supported by grants from Department of Atomic Energy, Department of Biotechnology and Department of Science and Technology, Government of India.

Access the paper titled "Major domestication-related phenotypes in indica rice are due to loss of miRNA-mediated laccase silencing" here.